Introduction
Palms
belong to the Arecaceae family, which comprises about 180 genera and
2600 species. They are ecologically and economically important as they provide
humans with medicine, food, and fuel and are commonly used for ornamental
purposes (Chao and Krueger 2007). Amongst
these species, three are most important, including date palm (Phoenix dactylifera
L.), coconut (Cocos nucifera L.), and the African oil palm (Elaeis
guineensis L.). Date palm is the most important fruit crop in the Middle
East, North Africa, and Arabian Peninsula. This crop was also introduced in
India, southern Africa, South America, Australia, and the United States. Based
on FAO statistics, date palm production significantly increased from 1.8
Million ton (Mt) in 1962 to 8.5 Mt in 2018, which Egypt been the first in date
production (1.6 Mt), followed by Saudi Arabia (1.3 Mt), Iran (1.2 Mt) and
Algeria (1.1 Mt) (FAO 2019). Coconut
palm, with a total cultivated area of 12 million ha and 62 million tone of
production, is grown in tropical areas (mainly in Asia) in 90 countries and it
is the main income source and staple food for many developing countries (FAO 2019). Oil palm production reached 272
Million tons in 2018 from about 19 million ha of cultivated area (FAO 2019).
Phytoplasmas are wall-less prokaryotes associated with
more than 600 diseases (Maejima et al. 2014; Kumari et al. 2019; Solomon et al.
2019). They are transmitted by phloem-sucking insects in the families
Cicadellidae, Cixiidae, Cercopidae, Derbidae, Delphacidae and Psyllidae (Weintraub and Beanland 2006; Linck and Reineke 2019;
Quaglino et al. 2019;
Jakovljević et al. 2020)
and colonize the vector by entering the midgut lumen, adhering to midgut
epithelium cells eventually invading the hemolymph and reaching the salivary
glands for further dissemination (Marzachì 2004).
There are several reports on the transovarial transmission of phytoplasmas to
the progeny by infected females (Kawakita et al. 2000; Tedeschi et al. 2006; Mittelberger et al. 2017).
In this review, up-to-date information is provided about
phytoplasma associated with palm diseases, vectors, management methods and
phytoplasma biology and interaction with palms.
Lethal
Yellowing Diseases
Lethal
yellowing diseases (LYD) are defined as a syndrome with similar and specific
symptoms (Gurr et al. 2016; Solomon et al.
2019). Lethal yellowing is also called lethal decline, lethal yellowing
type syndrome, and coconut lethal yellowing (Narvaez et al. 2016; Bahder et al. 2017). It is caused by many groups and subgroups of
phytoplasma in the world. The incidence and appearance of the symptoms vary
greatly depending on host species, variety, phytoplasma group, and geographical
location (Harrison et al. 2014). General symptoms observed in all LYD are the
drop of the immature and ripe fruits (Mazivele et al. 2018). The tips of the
fronds become yellow in color, especially on the oldest fronds, followed by
falling of fronds from the stem (Bila et al. 2019; Pilet et al. 2019; Solomon et al.
2019).
LYD was first observed and reported from the Caribbean
in the 1800s, followed by Ghana, Tanzania, and Togo (Dollet et al. 2009). An
outbreak of “coconut bud rot” resulted in extensive yield loss and stopped the
commercial production in the Caribbean (Johnson
1912). Simultaneously, an epidemic was reported from Jamaica, Honduras,
southern Mexico, Florida, Cuba, Haiti, Bahamas, and Belize (Harrison et al.
2002a; Baudouin et al. 2008; Lebrun et al. 2008; CABI 2012). Because
of the similarity of the typical symptoms in hosts in different parts of the
world, researchers suspected that they had the same causative agent. However,
the differences in symptom progression raised a question that there may be
different pathogens. The development in the identification techniques,
especially molecular identification, helped characterize the different groups
and subgroups of phytoplasma associated with this syndrome (Table 1) (Dollet et al.
2009; Eziashi and Omamor 2010; Bertaccini
et al. 2014; Contaldo et al.
2019; Córdova et al. 2019; Zamharir and
Eslahi 2019).
Currently, this disease is considered an important issue
in the coconut production industry in Central America and the Caribbean (Ntushelo et al.
2013). This disease is presently occurring in Nigeria, Mozambique,
Ghana, Benin, Lenya, Togo, Tanzania, India, Sri Lanka, Indonesia (Table 1) (Dollet et al.
2009; Eziashi and Omamor 2010; Perera et
al. 2012; Ramjegathesh et al.
2012, 2019). Smallholder and subsistence farmers were more affected by
the lethal yellowing disease due to their heavy reliance on coconut nutrition
and economy (Myrie et al. 2011).
LYD is widely reported from coconut (Fig. 1), although
it also occurs on date palm and oil palm (Kra et al. 2017; Zamharir and Eslahi 2019).
Table 1 presents the other palm species host of LYD. The most devastating
outbreak has been reported on coconut. For example, 86% of coconut trees died
from 1961 to 1983 in Jamaica (Jones 2002).
Other outbreaks referred to as “Akwa wilt”, “Cape St. Paul Wilt”, and
“Kian-cope” diseases killed millions of coconuts in Nigeria, Ghana, and Togo,
respectively (Eziashi and Omamor 2010).
It is estimated that 38% of coconut trees were destroyed in Tanzania since the
1960s (Mugini 2002). This disease is not
always “lethal”, and slight symptoms were observed in other species like date
palm (Manimekalai et al. 2014a; Zamharir and Eslahi 2019).
The first report of an association between phytoplasma
and date palm dates back to 1998 when Tymon et al. (1998) reported the
association of 16SrIV-C with silver date palms. Two years later, slow decline,
or El Arkish was reported from Sudan in which 16SrXIV was found associated with
this disease (Cronjé et al. 2000). In 2002, date palm yellows associated
with 16SrIV-A was reported from Kuwait (Al-Awadhi et al. 2002), which was the first
report of phytoplasma disease occurring in date palms in Asia. Al-Wijam
disease, associated with 16SrI-B phytoplasma, was observed in Saudi Arabia in
2007 (Alhudaib et al. 2007). In addition, the 16SrII phytoplasma has been
found associated with date palm in Saudi Arabia (Omar et al. 2018). In America,
16SrIV-F was first reported on date palm in 2013 (Ntushelo et al. 2013). Alkhazindar (2014) reported the association of
16SrI phytoplasma with date palm in Egypt. Recently, the 16SrVI-A and VII-A
phytoplasmas were reported on date palms in Iran (Zamharir et al. 2016; Zamharir
and Eslahi 2019). Although phytoplasma diseases on date palm are not
lethal so far, significant economic losses were observed in this region (Fig.
2). For example, fruit failure at harvest has been reported due to Al-Wijam in
Kuwait and Saudi Arabia (Alhudaib et al. 2007).
Origin and
causes of LYD
According to the report of LYD outbreak in the Caribbean, it is
speculated that the disease originated in this region (Johnson 1912). However, this hypothesis was rejected by Ogle and Harries (2005), who stated that
coconut palms were healthy after introduction to this region for several
hundred years in the 16th century. Importing grasses from India to
the Caribbean is the recent hypothesis indicating that insects harboring
phytoplasma could have transferred to the Caribbean on cattle fodder in the 19th
century. This speculation is supported by the fact that West Africa was the
destination of fodder transportation from India, where LYD occurred (Ogle and Harries 2005). Taking into account
the above facts, it can be hypothesized that the origin of LYD was in Asia (Ogle and Harries 2005). However, by the
identification and discovery of many associated phytoplasma groups with LYD, it
has been suggested that there were diverse origins. For instance, according to
the low mortality of Sabal Mexicana (Texas palmetto), Vázquez-Euán et
al. (2011) suggested the phytoplasma 16SrIV-D could have originated
in Mexico. Lethal yellowing disease occurred when a vector was introduced in
new areas indicating the non-native origin of the disease in the Caribbean (Elliott 2009), while the potential vectors of
the recent epidemic of Bogia coconut syndrome are all native species in Papua
New Guinea (Pilotti et al. 2014). Additional information regarding the
discovery and naming can be found in Lee et al. (2007).
Phytoplasmas are classified into groups and subgroups by
comprising the gene targeting the 16S ribosomal gene sequences. Currently, 44
groups and more than 100 subgroups have been identified and are yearly
increasing. In addition to this gene, other genes like tuf, secA, rp, groEL,
secY, and the 16S-23S rRNA spacer region are used for further distinction (Seruga Musić
et al. 2014; Al-Subhi et al.
2018; Balakishiyeva et al. 2018;
El-Sisi et al. 2018; Jamshidi et al. 2019; Oliveira et al. 2020). Also, specific
antibodies, vector transmission, and host range can be used for additional
discrimination (Fránová et al. 2013; Ntushelo et al.
2013).
Fig. 1: A map indicating distribution of
phytoplasma diseases in most important species of palms
Fig. 2: Symptoms of
yellowing and leaf stunting in Phoenix dactylifera associated with
16SrII-D phytoplasma
LYD Phytoplasmas are commonly classified into the 16SrIV
group, although some have now been reclassified into the groups 16SrXXII (Harrison et al.
2014), 16SrI, 16SrXI, and 16SrXIV (Bertaccini et al. 2014) (Fig. 3). Based on
vectors, plant hosts, and variety, the 16SrIV group is divided into six
subgroups A–F (Martinez et al. 2008; Vázquez-Euán et
al. 2011). These subgroups might vary in symptoms, host range, and
vectors. For instance, 16SrIV-A affect palms 18 months and older; another
subgroup of 16SrIV (not given) could infect bearing and non-bearing palms (Harrison et al.
2002b). Different phytoplasma groups have been reported in different
regions. For example, it has been demonstrated that the prevalent groups in
West and East Africa are XXII-B, IV-C, and a new unclassified
coconut-associated phytoplasma (Bila et al. 2015). On the other hand,
16SrXIV and 16SrXXIII groups have been reported from Malaysia (Nejat et al.
2009b).
Fig. 3: A phylogenetic
tree representing phytoplasma groups and subgroups associated with palms
Numerous plant species and/or varieties of palm are
infected with some phytoplasma subgroups (Table 1). In Mexico, 16SrIV-A is
found in T. radiate and C. nucifera in the same area, while Pseudophoenix
sargentii and S. mexicana are affected by 16SrIV-A. Also,
it is likely that one subgroup only infects a palm species (Table 1). However,
mixed infection with subgroups of a group in one palm species is not unexpected
as S. mexicanat could be a host of 16SrIV-D and 16SrIV-A (Fránová et al.
2013).
Spread of phytoplasma-associated palm diseases
LYD phytoplasmas
can be spread via different means. Oropeza et al. (2017) confirmed that
seed transmission could occur in LYD from embryos to plantlets by in vitro
germination of the zygotic embryo of infected seeds. Phytoplasmas can also
spread via movement of infected plant materials (Cordova et al. 2003). Geographical
barriers such as mountain ranges can significantly affect the rate of spread (CABI 2012). Human activity could play a
substantial role in the spread of plant diseases globally, including LYD. In
Mexico, for example, studies found that the export of palms and grasses from
Florida introduced LYD to Mexico before spreading to Central America. Other
diseases have been introduced to a new area in as the same scenario (Bertin et al.
2007).
Vectors
play a crucial role in phytoplasma distribution and spread (Rashidi et al.
2014; Linck and Reineke 2019). Although many papers have been published
on phytoplasma vectors, the vectors of many phytoplasmas Table 1: Current distribution, phytoplasma groups and host plants
of phytoplasma diseases on palms
Location |
Name |
16Sr Group |
Host |
References |
Asia |
||||
Iran |
Streak yellow date palm |
VI-A, VII-A |
Phoenix dactylifera |
(Zamharir and Eslahi 2019) |
Kuwait |
Yellows date palm |
IV-A |
P. dactylifera |
(Al-Awadhi et al. 2002) |
King Saudi Arabia |
Al-wijam |
I-B |
P. dactylifera |
(Alhudaib et al. 2007) |
lethal Yellowing palm disease |
II-D |
P. dactylifera |
(Omar et al. 2018) |
|
Lethal yellowing Mexican fan palm |
Washingtonia
robusta |
|||
India |
Kerala wilt disease |
IV-C |
Coconut
nucifera |
(Edwin and Mohankumar 2007) |
India |
Root (wilt) disease |
XI-A, XI-B |
C.
nucifera |
(Manimekalai et al. 2014b;
Yadav et al. 2015) |
India |
Oil palm stunting (OPS) |
I-B |
Elaeis
guineensis |
(Mehdi et al. 2012) |
Sri Lanka |
Weligama coconut leaf wilt disease |
XI |
C.
nucifera |
(Perera et al. 2012; Kumara et al. 2015) |
Malaysia |
Coconut yellow decline |
XIV |
C.
nucifera |
(Nejat et al. 2009a, c) |
Malaysia |
Ca. P. malayasianum |
XXXII-B, XXXII-C |
C.
nucifera, E. guineensis |
(Nejat et al. 2013) |
Malaysia |
Coconut lethal yellowing (CLY) |
XIV-A, I-B, XXXVI-A |
Wodyetia
bifurcata |
(Naderali et al. 2013, 2017) |
Malaysia |
Royal pam yellow decline |
I |
Roystonea
regia |
(Naderali et al. 2015) |
Malaysia |
Coconut yellow decline |
I-B |
Cyrtostachys renda |
(Naderali et al. 2014) |
Indonesia |
Kalimantan wilt and natura wilt |
XI, XIII |
C. nucifera |
(Ogle and Harries 2005; Warokka et
al. 2006) |
Africa |
||||
Nigeria |
Awka disease |
XXII-A |
C.
nucifera |
(Ekpo and Ojomo 1990; Tymon et al.
1998; Wei et al. 2007; Osagie et al. 2015) |
Tanzania |
Coconut lethal disease |
IV-C |
P.
dactylifera |
(Tymon et al. 1998) |
Kenya |
Coconut lethal disease |
IV-C |
C.
nucifera |
(Córdova et al. 2014) |
Mozambique |
Coconut lethal disease |
IV-B, IV-C,
XXII-A |
C.
nucifera |
(Córdova et al. 2014; Harrison et al. 2014; Bila et al. 2015) |
Ghana, Cote d’Ivoire, Nigeria, Togo, Cameron, Benin |
Cape St. Paul wilt, CSPW keta disease, Kinacope, Kribi
disease or Cote d’Ivoire lethal yellowing disease |
XXII-B, XXII-C |
C.
nucifera, Elaeis guineensis, Borasus aethiopium, Raphium vinifera |
(Harrison et al. 2014;
Arocha-Rosete et al. 2015; Osagie et al. 2015; Kra et al. 2017) |
Egypt |
Date palm yellows |
I-B |
P.
dactylifera |
(Alkhazindar 2014) |
Sudan |
Slow decline or El Arkish, or White Tip die-back |
XIV |
P.
dactylifera |
(Cronjé et al. 2000) |
America |
||||
Florida |
Coconut lethal yellowing (CLY) |
IV-F |
W.
robusta, P. dactylifera |
(Harrison et al. 2008;
Ntushelo et al. 2013) |
Dominican
Republic |
CLY |
IV-E |
C.
nucifera |
(Martinez et al. 2008;
Ntushelo et al. 2013; Córdova et al. 2014) |
Mexico, Honduras |
Yucatan coconut lethal decline, lethal yellowing
disease |
IV-B |
C.
nucifera, Acrocomia auleata |
(Roca et al. 2006; Ntushelo et al. 2013) |
Florida, Caribbean Basin |
CLY |
IV-A |
C.
nucifera and 38 other palm species |
(Gurr et al. 2016) |
Mexico, Texas
and Florida, Puerto Rico |
Texas Phoenix palm decline (TPPD) C. palmate
yellows (CPY) phytoplasma or Sabal Mexicana lethal decline, Lethal yellowing-like syndrom |
IV-D IV-A |
P.
canariensis, P. dactylifera, P. reclinata, P. roebelenii, P. sylvestria,
Sabal palmetto, Syagrus romanzoffiana, Carlodovica palmate, Sabal Mexicana,
Pseudophoenix sargentii, Pritchardia pacifica, Thrinzaradiata, Carpentaria
acuminate, Caryota mitis, Roystonea spp., Adonidia merrillee; Tharinax radiate, Coccothrinax readii; Roystonea regia; Acrocomia mexicana |
(Harrison et al. 2002c;
Narvaez et al. 2006; Vázquez-Euán et al. 2011; Córdova et al. 2014; Narvaez et al. 2016; Lara et al. 2017) |
Colombia |
Oil palm lethal wilt |
I-B |
Elaeis
guineensis |
(Alvarez et al. 2014) |
Florida (Hossonborg county) |
Lethal bronzing disease of palm |
IV-D |
Syagrus
romanzoffiana, Sabal palmetto |
(Bahder et al. 2018) |
Florida |
Texas phoenix palm decline (TPPD) |
IV-D |
Bismarckia
nubilis |
(Dey et al. 2018) |
Louisiana |
Lethal yellowing |
IV-A, IV_D |
P.
sylvestris; Trachycarpus fortunei |
(Singh and Ferguson 2017; Ferguson and Singh 2018) |
Cuba |
Lethal yellowing |
IV-A |
C.
nucifera |
(Llauger et al. 2002) |
Guatemala |
Lethal yellowing |
IV-A |
C.
nucifera |
(Mejía et al. 2004) |
Jamaica |
Lethal yellowing |
IV-A |
C.
nucifera |
(Myrie et al. 2007) |
Oceania |
||||
Papua new Guinea, Solomon Islands |
Banana wilt associated phytoplasma (BWAP) |
XXII-A |
C.
nucifera |
(Davis et al. 2015) |
still to be identified. Auchenorrhyncha and
Sternorrhyncha comprise most vectors of phytoplasmas (Howard et al. 2001).
Palms are hosts for many Auchenorrhyncha, although most of them do not cause a
direct injury. Having the ability to vector pathogens makes them the most
important threat to palms. Insects should be able to acquire and retransmit
phytoplasma to the healthy plants in order to be considered a vector (Bosco and Tedeschi 2013). The only confirmed
LYD vectors are Haplaxius crudus (van Duzee) in Florida (Howard et al.
1983) and Proutista moesta in India (Rajan 2013). Putative vectors of LYD
phytoplasmas are listed in Table 2.
Alternate
Hosts of LYD
Different
palm species and few non-palm related species are considered as alternative host
plants of LYD in Florida (Gurr et al. 2016; Rosete et al. 2016). Mixed infection of 16rXXII-A with a new group
of LYD was Table 2: A list of the
vectors of lethal yellowing disease
Location |
Disease
name/ Phytoplasma group |
Vector |
Testing
technique |
status |
references |
Florida |
Lethal
yellowing/16SrIV-A |
Haplaxius
crudus |
Cage
transmission test |
confirmed |
(Harrison et al.
2008) |
Mexico |
Lethal
yellowing/16SrIV-A, IV-D, IV-E |
H.
crudus |
Observation/PCR |
Suggested/Putative
|
(Córdova et al.
2014; Narváez et al. 2018) |
Ghana |
Cape
St. Paul Wilt/16SrXXII |
Myndus
apiopodoumensis |
Cage
trials were unsuccessful but detected positive in PCR |
Putative |
(Pilet et al.
2009) |
Mozambique |
Coconut
lethal yellow syndrome/ 16SrXXII |
Platacantha
lutea, Diostrombus mkurangai |
PCR |
Putative |
(Dollet et al.
2011; Bila et al. 2017) |
Tanzania |
Coconut
lethal disease/16SrIV-C |
Diastrombus
mkurangai |
PCR |
Putative |
(Mpunami et al.
2000) |
India |
Kerala
wilt disease |
Stephanitis
typical, Proutista
moesta, |
Cage
transmission |
Positive |
(Mathen et al.
1990) |
Sophonia
greeni |
Survey/
PCR |
Putative/negative |
(Rajan 2013) |
||
Sri
Lanka |
Weligama
coconut leaf wilt disease/16SrXI |
Zophiuma
pupillata |
PCR |
Putative |
(Pilotti et al.
2014) |
Cote
D’Ivoire |
Cote
D’Ivoire lethal yellowing/ 16SrXXII-B |
Nedutepa curta |
PCR |
Putative |
(Kwadjo et al.
2018) |
detected in
coconut farms near pine trees. The new group (closely related to Ca. P.
pini, 16SrXXI) is suggested to infect coconut palms as well as the pine (Bila et al.
2015). Attempts to find alternative host plants in Jamaica revealed that
some weeds being the host of 16SrIV-A, including Synderella nodiflora
and Emilia fosbergii. The number of alternative host plants
increased, in which Cleome rutidosperma, Stachytrapheta jamaicensis
and Macroptilium lathyroides were known to be infected by
16SrIV-E (Brown and McLaughlin 2011). Danyo (2011) reported Desmodium adscendeus
were positive in PCR when screening for alternative hosts for Cap St. Paul Wilt
disease.
In addition to the alternative hosts of phytoplasmas,
plants including acid limes grown under certain environmental conditions, are
subject to phytoplasma infection without developing disease symptoms (Marcone 2014; Al-Ghaithi et al. 2017). Detection phytoplasma in such plants by PCR
cannot specify if phytoplasma presence is for a short time feeding of the
visiting insects or if the plant is an actual alternative host of the
phytoplasma (Bertaccini et al. 2014). These plants may be considered more important
than the alternative hosts developing symptoms, as they may act as a source of
phytoplasma without been noticed.
Phytoplasma
Interaction with Vectors and Host Plants
Pacifico et al. (2015) suggested that phytoplasmas change their metabolism to
adapt to new hosts. Phytoplasma infection can alter the expression and
signaling level of host plant genes, which can affect plant development (Himeno et al.
2011; Bel and Musetti 2019; Wei et al.
2019; Parakkunnel et al. 2020).
Makarova
et al. (2015) studied the genomic response of the host plants and
vectors. They revealed that 34 genes in the vector and 74 genes in the host
plants were up regulated after infection, indicating the role of genes in host
adaptation. Nejat et al. (2015) revealed that coconut, ecotype Malayan Red
Dwarf, has downregulated more genes (21860 unigene) than the upregulated ones
(18013 unigene) in response to 16SIV-related strain infection. Most genes were
responsible for innate immunity, chlorosis, and biosynthesis of secondary
metabolites. The changes of endogenous cytokinin content in response to LYD
phytoplasma revealed that cytokinin levels drastically decreased in the
infected plants compared to the healthy ones (Aguilar et al. 2009). They stated that
the symptom appearance in the host plants is due to the changes in cytokinin
level.
Phytoplasmas live in the phloem and can be found in the
sieve elements of infected plants (Santi 2019;
Zimmermann et al. 2019). It
has been demonstrated that the disruption of the carbohydrate transport system
and the photosystem II reaction center efficiency by phytoplasmas result in LYD
symptoms (Maust et al. 2003). Coconut infected by RWB increased hydrogen
peroxide and super oxide anion (Sunukumar et al. 2014).
The relationship between the plant host and the vector
can play a crucial role in the disease management (Gonella et al. 2019; Tedeschi
and Bertaccini 2019; Weintraub et al.
2019). In epidemiology, the chance of outbreak will increase if there
are two factors, the completion of one generation of the vector, and
reacquiring phytoplasma from that plant host (Oppedisano et al. 2020). Some phytoplasma
can complete their generation on one non-crop species, and therefore, the plant
may die and acquiring phytoplasma by the vector will not occur. Bios Noir
(lethal disease of grapevines in Europe) is one example of this issue. Insect
vectors feeding on palms do not complete their life cycle. In addition, it has
been demonstrated that mature palms are susceptible to LYD. Some vector species
feed on only mature palm species and infrequently found on immature ones (Howard et al.
2001). On the other hand, BCS in PNG is susceptible at all growth stages
to LYD (Kelly
et al. 2011).
Transovarial transmission of phytoplasma in the vectors
has been recently reported (Alma et al. 2019; Tedeschi and Bertaccini
2019). Vectors harboring phytoplasma were reared, and offspring were
hatched and reared on healthy plants. The new nymphs were positive in PCR and
were able to transmit the phytoplasma to the new host plants (Hanboonsong et
al. 2002; Weintraub and Beanland 2006).
Mixed infection has been observed in polyphagous insect
vectors with closely related phytoplasmas (Brown et al. 2006; Rashidi et al. 2014). For example, Euscelidius
variegatus can acquire CYP (chrysanthemum yellows phytoplasma) and FDP
(Flavescence doreé phytoplasma). It has been reported that FDP can be affected
by CYP, and CYP was dominant in its body regardless of the order of infection.
Due to the facts that CYP had a shorter latent period and FDP cannot multiply
in the salivary gland, CYP is dominant than FDP in the vector body (Rashidi et al.
2014).
Some phytoplasmas have a positive relationship with their
vectors, which can be designated as mutualistic (Queiroz et al. 2016; Galetto et al. 2018). For example, AYPs
(Aster yellows phytoplasma) increased their host range preference as well as
the fecundity of the vector. Such a relationship shows that there is a
long-time association between them (Beanland et al. 2000; Ebbert and Nault 2001).
Conversely, some phytoplasmas decreased the fitness of the vector such as the
decrease in longevity, body size and fecundity (Malagnini et al. 2010; Mayer et al. 2011).
Infected host plants are more preferred by the vectors
as indicated in some pathosystems (MacLean et al. 2014; Krüger et al. 2015). Nevertheless, phytoplasma infected Cacopsylla
picta, the vector of “Ca. P. mali”, do not prefer to oviposit on
infected than un-infected trees (Mayer et al. 2011).
Management
Presently
there is no curative treatment for LYD, though some success in controlling the
outbreaks has been reported. An integrated pest and disease management
suggested by Black, a pioneer of palm growers, has been the most successful
approach in reducing the incidence of LYD (Gurr et al. 2016). This approach
focuses on on-farm quarantine, severe weekly surveillance, and cutting down and
burning of symptomatic palms. It is also recommended to plant resistant and
high yielding varieties, controlling weeds in the whole farm and using a good
fertilization schedule (Myrie et al. 2012). A significant
reduction in the number of LYD infected palms was observed in four farms using
Black’s method, while three farms continued to be destroyed by the disease
without any management. The farms with daily surveillance lost only 0.0001% (10
out of 62000) of palms, while other farms lost thousands of palms annually (Serju 2012).
To slow the spread of LYD, the eradication of the
infected palms is highly recommended in other parts of the world. This method
was used in the Dominican Republic, as they implemented an eradication program
combined with natural barriers stopping vector movement and profusion of
resistant palms (Martinez et al. 2008, 2010). Along with ground inspection in Ghana,
aerial surveillance was employed to detect infected palms showing green against
the yellow canopy of infected palms. Recently, the drone (crewless aerial
vehicles) equipped with cameras has come to help humans in large-scale surveys.
The instant eradication of infected trees and cultivation of a resistant
variety has slowed the spread of the disease (Nkansah-Poku et al. 2009). In addition, it
has been reported that farmers burn the felled trees in Jamaica (Serju 2012). This method has not effectively
slowed the spread, because the felled palms are not attractive to the vectors.
A research conducted by Nkansah-Poku et al. (2005) in Ghana revealed
that using insecticides followed by felling had no significant effect than
felling alone in stopping the spread.
Quarantine
LYD can
spread amongst close palm farms and also to hundreds of kilometers. Vector
movement can be prohibited by natural landscape barriers. However, human
activity can spread the disease even in the presence of barriers (Bertin et al.
2007). In Mexico, grasses are imported for landscaping, and the vectors
may come through this importation (Dollet et al. 2009), unless quarantine
measures are applied strictly.
Vector
management
Alternate
vector hosts
For the
univoltine vector, the control of alternative hosts of a vector can be the most
crucial approach of controlling phytoplasma diseases (Belien et al. 2013). For
instance, Haplaxius crudus nymphs, a known vector of LYD, feed and
develop on herbaceous plants root, while the adults live on trees and palms (Howard 1995). Four species of Cyperaceae and
37 species of Poaceae were identified to be the host of H. crudus
nymphs. Grasses which are not potential host and shade-tolerant can be selected
to be replaced with alternative hosts. Howard
(1995) introduced some species that can be planted under palms as
non-hosts, including Hemarthria altissima (Pior), Brachiaria
brizantha (A. Rich) and Chloris gayana Kunth.
Mulches could be considered as a control approach. For
instance, mulches of subtle pine, coconut frond, and eucalyptus are more
attractive for female oviposition. Also, they provide better conditions for
developing nymphs, resulting in higher adult emergence. On the other hand,
using bark nuggets can result in less adult emergence (Howard and Oropeza 1998). It can be noted that mulch application
is too expensive and practical.
Insecticides
Palms are evergreen
and long living, so the vectors are able to transmit phytoplasmas anytime,
contrary to temperate, and annul crops needing protection only for short times
of susceptibility (Gitau et al. 2009). Palms are the host of many insect species, so
the use of broad-spectrum insecticides can destroy the food chain of
parasitoids and predators. In addition, the wider environment and human health
are threatened by persistent pesticides (Stehle
and Schulz 2015; Gangireddygari et al.
2017). Trunk injection and spraying insecticides are used for
controlling the vector, although it has not been economically successful in
coconut farms (Been 1995). Similarly, the
control of Kerala Wilt Disease (KWD) in India was not successful using
insecticides (Rajan 2013). In addition, a similar result was reported in
Florida where the population of the vector and spread of the disease was
reduced, but without stopping infection (Been
1995).
Host plant
resistance
Jarausch et al. (2013) defined resistant and tolerant cultivars as the absence
of symptoms associated with a low pathogen titer in the infected plants and
mild symptoms under a light pathogen titer, respectively. It should be noted
that complete resistance to LYD phytoplasma has not been reported (Baudouin et al.
2009).
As palms have to pass more time to be reproducible as
well as produce few seeds per plant, genetic modifications and improvements are
so difficult (Cardeña et al. 2003). Also, because the latent period in palms is
long, resistance screening of current genotypes is also difficult. However,
detection of phytoplasma can be more accessible, reliable, and faster by PCR
technology (Valiunas et al. 2019; Gholami et al.
2020; Wang et al. 2020). It
has been documented that the level of resistance can be affected by environmental
conditions (Baudouin et al. 2009). In some cases, it has been observed that
resistance depends on environmental factors than genetic as the speculated
resistant cultivars were infected in some regions, while on the other hand they
were resistant in some other regions (Mpunami et al. 1999; Mpunami et al. 2002). In addition, a
palm resistant to some strains will be likely threatened by a different group
and subgroup of phytoplasma even by a new vector when planted in a new region (Odewale et al.
2012).
Information about the rate of mutations in phytoplasma
is scarce due to the difficulty to culture these pathogens. In addition, no evidence is available on the effects of
transmission or vectors on mutations in phytoplasmas. On the other hand, a
study has shown that an induced mutation in the onion yellowing phytoplasma
resulted in the loss of transmission ability of its insect vector compared to
the wild type (Oshima et al. 2004).
There are several virulence factors in
phytoplasmas including SAP11, SAP54, PHYL1 and TENGU, which can induce specific
symptoms in the diseased plants. It has been shown that a mutation in the
virulence factor TENGU resulted in plant resistance to insect vectors. The
mutant phytoplasma could not change the color of the leaves and with such
symptoms, the vectors were not attracted to the plants (Sugio et al.
2014). However, there is no documented literature on the effects of mutations
in virulence factors on the breakdown of resistance.
Transmission trials with insect vectors are more
reliable and real for resistance screening, though a distinction between
resistance to the vector or the phytoplasma is so difficult (Jarausch et al.
2013). In this way, the population dynamics of the vector needs to be
monitored. To test resistance in coconut, researchers test different varieties
in which LYD is endemic (Baudouin et al. 2009; Odewale and Okoye 2013).
To search for resistant varieties, the researchers plant
a range of resistant varieties in any growing area. Such a method is used to make
plant adaptation to the phytoplasma or vector population. However, after a
period, the resistance may breakdown, and symptoms of the disease appear (Quaicoe et al.
2009). Variety evaluation and improvements should be carried out in the
area as resistance has a degree of site-specificity, which may be affected by
environmental factors, especially drought and poor soil conditions, and genetic
variation between phytoplasma populations (Odewale et al. 2012). Adaption in
phytoplasma may occur fast due to repetitive genomes and short time generation.
Gene stacking has been newly suggested in order to stop resistance breaking
down; however, no published work is available on the use
of gene stacking to manage phytoplasmas in palms. CRISPR (Cluster
Regulatory Interspaced Short Palindromic Repeats) is the newest tool for gene
editing (Abdelrahman et al. 2018; Ipoutcha et al.
2019). By this method, phytoplasma resistance traits can be easily known
and exploited for by gene silencing or insertion (Belhaj et al. 2013).
The most important challenge in host plant resistance in
LYD management might be that such resistance to phytoplasma pathogen may change
the susceptibility to other pathogens or pests. For instance, the resistance
cultivars in PNG became more susceptible to two pests, including black palm
weevil Rhynocophorus bilineatus (Montr.) and Oryctes rhinoceros
(Ovasuru 1994).
Despite the challenges mentioned, such an approach was
used in LYD management. For example, CSPWD (Cape Saint Paul Wilt Disease) was
controlled using a hybrid of Vanuata Tall, and Sri Lanka Green Dwarf in Ghana (Quaicoe et al.
2009). Also, Jamaican farmers replaced the Maypan and Malayan dwarf
varieties by a tall variety, which resulted in retrieval of the coconut
industry (Harrison et al. 2002a).
Although replanting the cultivars may be costly and
practical, this method can help the coconut industry as the average age of many
plants in many parts is old. However, the long period, in which coconut last
for sufficient production should be considered (Danyo
2011; Snaddon et al. 2013).
Antibiotic
treatment
Using
antibiotics can prevent or control phytoplasma infection in individual host
plants (Tanno
et al. 2018; Bogoutdinov et al.
2019). To get better results, antibiotics must be used bi-weekly for
four months by systemic treatment. This method is costly and cannot be used in
commercial production; however, it can be applied for beneficial and decorative
palms in hotels or tourist sites (Eziashi and
Omamor 2010). However, the use of antibiotics is forbidden in developed
countries (Musetti et al. 2013). Because of the perceived health risks and
cost of this approach, antibiotics can be used to protect cherished ornamental
trees but have never been considered as a continuous way of management (Been 1995).
Effect of
Abiotic factors and climate change on LYD
Little
relative information is available on how LYD may be affected by abiotic factor.
It was well known that moisture and temperature can affect the severity of
associated phytoplasma (Krishnareddy 2013).
As demonstrated in some studies, disruption in stomata can contribute to
excessive water loss and leaflet flaccidity in palm root wilt (Rajagopal et
al. 1986). Mulches and the density of host plants and the distance
between coconut plantations could affect vector biology and ecology. The spread
of LYD can be affected by landscape and climate (Mora-Aguillera
2002). Researches on “flavescene doreé” and chrysanthemum yellows
revealed that multiplication in insects was faster under cooler with a low CO2
concentration condition (18–22°C; CO2 400); contrary to plants (22–26°C; 800 ppm)
(Galetto
et al. 2011).
The establishment and spread of the phytoplasma vectors
and associated phytoplasma might change due to climate change (Krishnareddy 2013). One centigrade increase in
temperature resulted in shifting ecological zone by up to 160 km, as stated by Thuiller (2007). It has been known that an
increase in temperature may result in insect species spread into new areas and
even new countries (Parmesan and Yohe 2003).
Transmission success may be increased by higher feeding
frequency or faster multiplication in the host due to an increase in
temperature, which may increase the rate of spread of the phytoplasma (Maggi et al.
2014). In the case of LYD, it is so difficult to predict the
consequences of climate change accurately due to lacking the information of the
temperature range of LYDs. Halbert et al. (2014) demonstrated that
LYD phytoplasma could overwinter consistently further north (N29°), therefore
the LYD spread depends on insect physiology rather than ecology.
Conclusion
Phytoplasma
diseases of palms are economically destructive diseases, which have resulted in
significant effects on humans’ economy and nutrition. There are many gaps in
understanding the phytoplasma diseases of palms, including epidemiology,
biology of the phytoplasmas, ecology and the biology of the vector, and the
relationship between the hosts, vector and pathogen. This question opens a
window for further investigation. Vectors play a crucial role in epidemiology.
However, vertical transmission of phytoplasma in plant hosts has been
confirmed. Proper quarantine and seed movement policies are needed to prevent
disease spread. Although many attempts have been ongoing for the identification
of the vectors species, little information is still available. It should be
noted that a transmission trial to confirm a vector is logistically
challenging. In disease management, early detection of the disease and vector
can help implement the best approaches and prevent disease spread. This issue
has been solved by recent quick techniques in detection such as Polymerase
Chain Reaction (PCR), Loop-mediated isothermal amplification (LAMP), and
digital PCR (dPCR).
Acknowledgments
Authors
would like to thank Sultan Qaboos University and VALE Oman for financial
support of the phytoplasma studies.
References
Abdelrahman M, AM Al-Sadi, A
Pour-Aboughadareh, DJ Burritt, LSP Tran (2018). Genome editing using
CRISPR/Cas9–targeted mutagenesis: An opportunity for yield improvements of crop
plants grown under environmental stresses. Plant
Physiol Biochem 131:31‒36
Aguilar ML, F Espadas, B Maust, L Sáenz
(2009). Endogenous cytokinin content in coconut palms affected by lethal
yellowing. J Plant Pathol 91:141‒146
Al-Awadhi HA, A Hanif, P Suleman, MS
Montasser (2002). Molecular and microscopical detection of phytoplasma
associated with yellowing disease of date palms Phoenix dactylifera L. in Kuwait. Kuw J Sci Eng 29:87‒109
Al-Ghaithi AG, AM Al-Sadi, MS Al-Hammadi,
RM Al-Shariqi, RA Al-Yahyai, IH Al-Mahmooli, CM Carvalho, SL Elliot, S Hogenhout (2017).
Expression of phytoplasma-induced
witches’ broom disease symptoms in acid lime (Citrus aurantifolia) trees is affected by climatic conditions. Plant Pathol 66:1380‒1388
Al-Subhi AM, SA Hogenhout, AM Al-Sadi, RA
Al-Yahyai (2018). Detection, identification, and molecular characterization of
the 16SrII-D phytoplasmas infecting vegetable and field crops in Oman. Plant Dis 102:576‒588
Alhudaib K, Y Arocha, M Wilson, P Jones
(2007). "Al-Wijam", a new phytoplasma disease of date palm in Saudi
Arabia. Bull Insectol 60:285‒286
Alkhazindar M (2014). Detection and
molecular identification of aster yellows phytoplasma in date palm in Egypt. J Phytopathol 162:621‒625
Alma A, F Lessio, H Nickel (2019). Insects
as phytoplasma vectors: Ecological and epidemiological aspects. In:
Phytoplasmas: Plant Pathogenic Bacteria - II: Transmission and Management of
Phytoplasma - Associated Diseases, pp:1‒25. Springer, Singapore
Alvarez E, JF Mejía, N Contaldo, S
Paltrinieri, B Duduk, A Bertaccini (2014). 'Candidatus
phytoplasma asteris' strains associated with oil palm lethal wilt in Colombia. Plant Dis 98:311‒318
Arocha-Rosete Y, JL Konan-Konan, AH
Diallo, K Allou, J Scott (2015). Analyses based on the 16S rRNA and secA genes
identify a new phytoplasma subgroup associated with a lethal yellowing-type
disease of coconut in Côte d'Ivoire. Phytopathog
Mollic 5:57–60
Bahder BW, EE Helmick, S Chakrabarti, S
Osorio, N Soto, T Chouvenc, NA Harrison (2018). Disease progression of a lethal
decline caused by the 16SrIV-D phytoplasma in Florida palms. Plant Pathol 67:1821‒1828
Bahder BW, EE Helmick, NA Harrison (2017).
Detecting and differentiating phytoplasmas belonging to subgroups 16SrIV-A and
16SrIV-D associated with lethal declines of palms in florida using qPCR and
high-resolution melt analysis (HRMA). Plant
Dis 101:1449‒1454
Balakishiyeva G, J Bayramova, A Mammadov,
P Salar, JL Danet, I Ember, E Verdin, X Foissac, I Huseynova (2018). Important
genetic diversity of ‘Candidatus
Phytoplasma solani’ related strains associated with bois noir grapevine yellows
and planthoppers in Azerbaijan. Eur J
Plant Pathol 151:937‒946
Baudouin L, R Philippe, R Quaicoe, S Dery,
M Dollet (2009). General overview of genetic research and experimentation on
coconut varieties tolerant/resistant to Lethal Yellowing. Oléag Corps Gras Lipid 16:127‒131
Baudouin L, P Lebrun, A Berger, W Myrie, B
Been, M Dollet (2008). The Panama Tall and the Maypan hybrid coconut in
Jamaica: Did genetic contamination cause a loss of resistance to Lethal
Yellowing? Euphytica 161:353‒360
Beanland L, CW Hoy, LR Nault (2000).
Influence of aster yellows phytoplasma on the fitness of Aster Leafhopper
(Homoptera: Cicadellidae). Ann Entomol
Soc Amer 93:271‒276
Been BO (1995). Integrated pest management
for the control of lethal yellowing: Quarantine, cultural practices and optimal
use of hybrids. In: Lethal Yellowing: Research and Practical Aspects,
pp:101‒109. Oropeza C, FW Howard, GR Ashburner (Eds.). Kluwer Academic
Publishers, Dordrecht, The Netherlands
Bel AJEV, R Musetti (2019). Sieve element
biology provides leads for research on phytoplasma lifestyle in plant hosts. J Exp Bot 70:3737‒3755
Belhaj K, A Chaparro-Garcia, S Kamoun, V
Nekrasov (2013). Plant genome editing made easy: Targeted mutagenesis in model
and crop plants using the CRISPR/Cas system. Plant Meth 9:1‒10
Belien T, E Bangels, G Peusens (2013).
Integrated control of psyllid vectors of European fruit tree phytoplasmas. Phytopathog Mollic 3:31‒36
Bertaccini A, B Duduk, S Paltrinieri, N
Contaldo (2014). Phytoplasmas and phytoplasma diseases: A severe threat to
agriculture. Amer J Plant Sci 5:1763‒1788
Bertin S, CR Guglielmino, N Karam, LM
Gomulski, AR Malacrida, G Gasperi (2007). Diffusion of the nearctic leafhopper Scaphoideus titanus Ball in Europe: A
consequence of human trading activity. Genetica
131:275‒285
Bila J, A Mondjana, L Santos, N Högberg
(2019). Coconut lethal yellowing disease and the oryctes monoceros beetle: A
joint venture against coconut production in Mozambique. Phytopathog Mollic 9:153‒154
Bila J, A Mondjana, B Samils, N Högberg,
MR Wilson, L Santos (2017). First report of ‘Candidatus phytoplasma palmicola’ detection in the planthopper Diostrombus mkurangai in Mozambique. Bull Insectol 70:45‒48
Bila J, A Mondjana, B Samils, N Högberg
(2015). High diversity, expanding populations and purifying selection in
phytoplasmas causing coconut lethal yellowing in Mozambique. Plant Pathol 64:597‒604
Bogoutdinov DZ, TB Kastalyeva, NV Girsova,
LN Samsonova (2019). Phytoplasma diseases: A review of 50 year history and
current advances. Sel'skokhozyaist Biol
54:3‒18
Bosco D, R Tedeschi (2013). Insect vector
transmission assays. In: Methods in Molecular Biology, pp:73‒85.
Humana Press Inc., New Jersey, USA
Brown SE, WA McLaughlin (2011).
Identification of lethal yellowing group (16SrIV) of phytoplasmas in the weeds Stachytarpheta jamaicensis, Macroptilium lathyroides and Cleome rutidosperma in Jamaica. Phytopathog Mollic 1:27‒34
Brown SE, BO Been, WA McLaughlin (2006).
Detection and variability of the lethal yellowing group (16Sr IV) phytoplasmas
in the Cedusa spp. (Hemiptera:
Auchenorrhyncha: Derbidae) in Jamaica. Ann
Appl Biol 149:53‒62
CABI (2012). “Candidatus Phytoplasma palmae". In: Invasive Species
Compendium. Wallingford, UK, CAB International UK
Cardeña R, GR Ashburner, C Oropeza (2003).
Identification of RAPDs associated with resistance to lethal yellowing of the
coconut (Cocos nucifera L.) palm. Sci Hortic 98:257‒263
Chao CT, RR Krueger (2007). The date palm
(Phoenix dactylifera L.): Overview of biology, uses, and cultivation. Hortscience 42:1077‒1082
Contaldo N, G D'Amico, S Paltrinieri, HA
Diallo, A Bertaccini, Y Arocha Rosete (2019). Molecular and biological
characterization of phytoplasmas from coconut palms affected by the lethal
yellowing disease in Africa. Microbiol
Res 223–225:51‒57
Cordova I, P Jones, NA Harrison, C Oropeza
(2003). In situ PCR detection of phytoplasma DNA in embryos from coconut palms
with lethal yellowing disease. Mol Plant
Pathol 4:99‒108
Córdova I, C Oropeza, N Harrison, S
Ku-Rodríguez, C Puch-Hau, M Narváez, L Sáenz (2019). Simultaneous detection of
coconut lethal yellowing phytoplasmas (group 16SrIV) by real-time PCR assays
using 16Sr- and GroEL-based TaqMan probes. J
Plant Pathol 101:609‒619
Córdova I, C Oropeza, C Puch-Hau, N
Harrison, A Collí-Rodríguez, M Narvaez, G Nic-Matos, C Reyes, L Sáenz (2014). A
real-time pcr assay for detection of coconut Lethal yellowing Phytoplasmas of
group 16sriv subgroups A, D and E found in the Americas. J Plant Pathol 96:343‒352
Cronjé P, AJ Dabek, P Jones, AM Tymon
(2000). Slow decline: A new disease of matare date palms in North Africa
associated with a phytoplasma. Plant
Pathol 49:804
Danyo G (2011). Review of scientific
research into the Cape Saint Paul Wilt Disease (CSPWD) of coconut in Ghana. Afr J Agric Res 6:4567‒4578
Davis RI, J Henderson, LM Jones, AR
McTaggart, C O’Dwyer, F Tsatsia, C Fanai, JB Rossel (2015). First record of a
wilt disease of banana plants associated with phytoplasmas in Solomon Islands. Aust Plant Dis Notes 10:14–20
Dey KK, A Jeyaprakash, J Hansen, D Jones,
T Smith, D Davison, P Srivastava, B Bahder, C Li, X Sun (2018). First report of
the 16SrIV-D phytoplasma associated with decline of a Bismarck palm (Bismarckia nobilis). Plant Health Progr 19:128‒128
Dollet M, F Macome A Vaz, S Fabre (2011).
Phytoplasmas identical to coconut lethal yellowing phytoplasmas from Zambesia
(Mozambique) found in a pentatomide bug in Cabo Delgado province. Bull Insectol 64:139‒140
Dollet M, R Quaicoe, F Pilet (2009). Review
of coconut "lethal yellowing" type diseases diversity, variability
and diagnosis. Oleag Corps Gras Lipid
16:97‒101
Ebbert MA, LR Nault (2001). Survival in
Dalbulus leafhopper vectors improves after exposure to maize stunting
pathogens. Entomol Exp Appl 100:311‒324
Edwin BT, C Mohankumar (2007). Kerala wilt
disease phytoplasma: Phylogenetic analysis and identification of a vector,
Proutista moesta. Physiol Mol Plant
Pathol 71:41‒47
Ekpo EN, EE Ojomo (1990). The spread of
lethal coconut diseases in West Africa: Incidence of Awka disease (or bronze
leaf wilt) in the Ishan area of Bendel state of Nigeria. Principes 34:143‒146
El-Sisi Y, AF Omar, SA Sidaros, MM
Elsharkawy, X Foissac (2018). Multilocus sequence analysis supports a low
genetic diversity among ‘Candidatus
Phytoplasma australasia’ related strains infecting vegetable crops and
periwinkle in Egypt. Eur J Plant Pathol
150:779‒784
Elliott ML (2009). Emerging palm diseases
in Florida. HortTechnology 19:717‒718
Eziashi E, I Omamor (2010). Lethal yellowing
disease of the coconut palms (Cocos
nucifera L.): An overview of the crises. Afr J Biotechnol 9:9122‒9127
FAO (2019). FAOSTAT [Online]. FAO.
Available: http://www.fao.org/faostat/en/#data/QC/visualize [Accessed
8/12/2019]
Ferguson MH, R Singh (2018). First report
of lethal yellowing associated with phytoplasma subgroup 16SrIV-A on silver
date palm and Chinese windmill palm in Louisiana. Plant Dis 102:2028‒2028
Fránová J, H Ludvíková, F Paprštein, A
Bertaccini (2013). Genetic diversity of Czech 'Candidatus Phytoplasma mali' strains based on multilocus gene
analyses. Eur J Plant Pathol 136:675‒688
Galetto L, S Abbà, M Rossi, M Vallino, M
Pesando, N Arricau-Bouvery, MP Dubran, W Chitarra, M Pegoraro, D Bosco, C
Marzachì (2018). Two phytoplasmas elicit different responses in the insect
vector Euscelidius variegatus
Kirschbaum. Infect Immun 86:42–62
Galetto L, C Marzachì, R Marques, C
Graziano, D Bosco (2011). Effects of temperature and CO2 on
phytoplasma multiplication pattern in vector and plant. Bull Insectol 64:151‒152
Gangireddygari VSR, PK Kalva, K Ntushelo,
M Bangeppagari, AD Tchatchou, RR Bontha (2017). Influence of environmental
factors on biodegradation of quinalphos by Bacillus thuringiensis. Environ Sci Eur 29:11–21
Gholami J, M Bahar, M Talebi (2020). Simultaneous
Detection and Direct Identification of Phytoplasmas in the Aster Yellows
(16SrI), Clover proliferation (16SrVI) and stolbur (16SrXII) groups using a Multiplex
Nested PCR assay in potato plants. Potato
Res 2020: https://doi.org/10.1007/s11540-019-09447-8
Gitau CW, GM Gurr, CF Dewhurst, MJ
Fletcher, A Mitchell (2009). Insect pests and insect-vectored diseases of
palms. Aust J Entomol 48:328‒342
Gonella E, R Musetti, E Crotti, M Martini,
P Casati, E Zchori-Fein (2019). Microbe relationships with phytoplasmas in
plants and insects. In: Phytoplasmas: Plant Pathogenic Bacteria - II:
Transmission and Management of Phytoplasma - Associated Diseases, pp:207‒235.
Springer, Singapore
Gurr GM, AC Johnson, GJ Ash, BAL Wilson,
MM Ero, CA Pilotti, CF Dewhurst, MS You (2016). Coconut lethal yellowing
disease: A phytoplasma threat to palms of global economic and social
significance. Front Plant Sci 7;
Article 1521
Halbert SE, SW Wilson, B Bextine, SB
Youngblood (2014). Potential planthopper vectors of palm phytoplasmas in
Florida with a description of a new species of the genus omolicna (Hemiptera: Fulgoroidea). Flor Entomol 97:90‒97
Hanboonsong Y, C Choosai, S Panyim, S
Damak (2002). Transovarial transmission of sugarcane white leaf phytoplasma in
the insect vector Matsumuratettix
hiroglyphicus (Matsumura). Insect Mol
Biol 11:97‒103
Harrison NA, RE Davis, C Oropeza, EE
Helmick, M Narváez, S Eden-Green, M Dollet, M Dickinson (2014). 'Candidatus Phytoplasma palmicola',
associated with a lethal yellowing-type disease of coconut (Cocos nucifera L.) in Mozambique. Intl J Syst Evol Microbiol 64:1890‒1899
Harrison NA, EE Helmick, ML Elliott
(2008). Lethal yellowing-type diseases of palms associated with phytoplasmas
newly identified in Florida, USA. Ann
Appl Biol 153:85‒94
Harrison NA, W Myrie, P Jones, ML Carpio,
M Castillo, MM Doyle, C Oropeza (2002a). 16S rRNA interoperon sequence
heterogeneity distinguishes strain populations of palm lethal yellowing
phytoplasma in the Caribbean region. Ann
Appl Biol 141:183‒193
Harrison NA, M Narváez, H Almeyda, I
Cordova, ML Carpio, C Oropeza (2002b). First report of group 16SrIV
phytoplasmas infecting coconut palms with leaf yellowing symptoms on the
Pacific coast of Mexico. Plant Pathol
51:808-808
Harrison NA, M Womack, ML Carpio (2002c).
Detection and characterization of a lethal yellowing (16SrIV) group phytoplasma
in Canary Island date palms affected by lethal decline in Texas. Plant Dis 86:676‒681
Himeno M, Y Neriya, N Minato, C Miura, K
Sugawara, Y Ishii, Y Yamaji, S Kakizawa, K Oshima, S Namba (2011). Unique
morphological changes in plant pathogenic phytoplasma-infected petunia flowers
are related to transcriptional regulation of floral homeotic genes in an
organ-specific manner. Plant J 67:971‒979
Howard FW (1995). Lethal yellowing vector
studies. II. Status of Myndus crudus host plant studies. In: Lethal
Yellowing: Research and Practical Aspects, pp:59‒64. Oropeza C, FW
Howard, GR Ashburner (Eds.). Kluwer Academic Publishers, Dordrecht, The
Netherlands
Howard FW, C Oropeza (1998). Organic mulch
as a factor in the nymphal habitat of Myndus
crudus (Hemiptera: Auchenorrhyncha: Cixiidae). Flor Entomol
81:92‒97
Howard FW, D Moore, RM Giblin-Davis, RG
Abad (2001). The animal class Insecta and the plant family Palmae. In:
Insects on Palms, pp:1‒32. New York, CAbI Publishing New York, USA
Howard FW, R Norris, D Thomas (1983).
Evidence of transmission of palm lethal yellowing agent by a planthopper, Myndus crudus (Homoptera, Cixiidae). Trop Agric 60:168‒171
Ipoutcha T, I Tsarmpopoulos, V Talenton, C
Gaspin, A Moisan, CA Walker, J Brownlie, A Blanchard, P Thebault, P
Sirand-Pugnet (2019). Multiple Origins and Specific Evolution of CRISPR/Cas9
Systems in Minimal Bacteria (Mollicutes).
Front Microbiol 10; Article 2701
Jakovljević M, J Jović, O
Krstić, M Mitrović, S Marinković, I Toševski, T Cvrković
(2020). Diversity of phytoplasmas identified in the polyphagous leafhopper Euscelis incisus (Cicadellidae, Deltocephalinae)
in Serbia: Pathogen inventory, epidemiological significance and vectoring
potential. Eur J Plant Pathol 156:201‒221
Jamshidi E, S Murolo, SB Ravari, M Salehi,
G Romanazzi (2019). Molecular Typing of 'Candidatus Phytoplasma solani'
in Iranian Vineyards. Plant Dis 103:2412‒2416
Jarausch W, E Angelini, S Eveillard, S Malembic-Maher (2013).
Management of fruit tree and grapevine phytoplasma diseasethrough genetic
resistance. In: New Perspectives in Phytoplasma Disease Management, pp:56‒62.
Torres E, A Laviña, W Jarausch, A Bertaccini (Eds.). COST Action FA0807,
Barcelona, Spain
Johnson JR (1912). The History and Cause of Coconut Bud-Rot, USDA Bureau of Plant
Industry Bulletin NO. 228, Washington DC, USA
Jones P (2002). Phytoplasma plant
pathogens. In: Plant Pathologist’s Pocketbook, pp:126‒139. Waller
JM, JM Lenné, SJ Waller (Eds.). CABI Publishing, Wallingford, UK
Kawakita H, T Saiki, W Wei, W Mitsuhashi,
K Watanabe, M Sato (2000). Identification of mulberry dwarf phytoplasmas in the
genital organs and eggs of leafhopper Hishimonoides sellatiformis. Phytopathology 90:909‒914
Kelly PL, R Reeder, P Kokoa, Y Arocha, T
Nixon, A Fox (2011). First report of a phytoplasma identified in coconut palms
(Cocos nucifera) with lethal yellowing-like symptoms in Papua New
Guinea. New Dis Rep 23:9-9
Kra KD, MNY Toualy, AEP Kouamé, K Séka, KE
Kwadjo, HA Diallo, A Bertaccini, Y Arocha-Rosete (2017). New phytoplasma
subgroup identified from Arecaceae palm species in Grand-Lahou, Côte d’Ivoire. Can J Plant Pathol 39:297‒306
Krishnareddy M (2013). Impact of climate
change on insect vectors and vector-borne plant viruses and phytoplasma. In:
Climate-Resilient Horticulture: Adaptation and Mitigation Strategies, pp:255‒277.
Springer, New Delhi, India
Krüger K, F Venter, ML Schröder (2015).
First insights into the influence of aster yellows phytoplasmas on the
behaviour of the leafhopper Mgenia
fuscovaria. Phytopathog Mollic 5:41‒42
Kumara ADNT, L Perera, MK Meegahakumbura, NS Aratchige, LCP
Fernando (2015). Identification of putative vectors of weligama coconut leaf wilt
disease in Sri Lanka. In: New Horizons in Insect Science: Towards
Sustainable Pest Management New Delhi, Chakravarthy, AK (Eds.). Springer,
Dordrecht, The Netherlands
Kumari S, K Nagendran, AB Rai, B Singh, R
Govind Pratap, A Bertaccini (2019). Global status of phytoplasma diseases in
vegetable crops. Front Microbiol 10;
Article 1349
Kwadjo KE, NDI Beugré, CH Dietrich, ATT
Kodjo, HA Diallo, N Yankey, S Dery, M Wilson, JLK Konan, N Contaldo, S
Paltrinieri, A Bertaccini, YA Rosete (2018). Identification of Nedotepa curta
Dmitriev as a potential vector of the Côte d'Ivoire lethal yellowing
phytoplasma in coconut palms sole or in mixed infection with a ‘Candidatus Phytoplasma asteris’-related
strain. Crop Prot 110:48‒56
Lara IC, LM Narváez, CP Hau, C Oropeza, L
Sáenz (2017). Detection and identification of lethal yellowing phytoplasma
16SrIV-A and D associated with Adonidia
merrillii palms in Mexico. Aust Plant
Pathol 46:389‒396
Lebrun P, L Baudouin, W Myrie, A Berger, M
Dollet (2008). Recent lethal yellowing outbreak: Why is the Malayan Yellow
Dwarf Coconut no longer resistant in Jamaica? Tree Genet Genomics 4:125‒131
Lee IM, Y Zhao, RE Davis, W Wei, M Martini
(2007). Prospects of DNA-based systems for differentiation and classification
of phytoplasmas. Bull Insectol 60:239‒244
Linck H, A Reineke (2019). Preliminary
survey on putative insect vectors for Rubus stunt phytoplasmas. J Appl Entomol 143:328‒332
Llauger R, D Becker, J Cueto, E Peralta, V
González, M Rodríguez, W Rohde (2002). Detection and molecular characterization
of phytoplasma associated with Lethal Yellowing disease of coconut palms in
Cuba. J Phytopathol 150:390‒395
MacLean AM, Z Orlovskis, K Kowitwanich, AM
Zdziarska, GC Angenent, RGH Immink, SA Hogenhout (2014). Phytoplasma effector
SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes
insect colonization in a RAD23-dependent manner. PLoS Biol 12; Article e1001835
Maejima K, K Oshima, S Namba (2014).
Exploring the phytoplasmas, plant pathogenic bacteria. J Gen Plant Pathol 80:210‒221
Maggi F, D Bosco, C Marzachi (2014). Conceptual and mathematical modeling of
insect-borne plant diseases: Theory and application to Flavescence doree in
grapevine, pp:1‒31. Research Report, Department of Civil Engineering,
University of Sydney, Australia
Makarova O, AM MacLean, M Nicolaisen
(2015). Phytoplasma adapt to the diverse environments of their plant and insect
hosts by altering gene expression. Physiol
Mol Plant Pathol 91:81‒87
Malagnini V, F Pedrazzoli, V Gualandri, F
Forno, R Zasso, A Pozzebon, C Ioriatti (2010). A study of the effects of 'Candidatus Phytoplasma mali' on the
psyllid Cacopsylla melanoneura
(Hemiptera: Psyllidae). J Invertebr
Pathol 103:65‒67
Manimekalai R, S Nair, VP Soumya (2014a).
Evidence of 16SrXI group phytoplasma DNA in embryos of root wilt diseased
coconut palms. Aust Plant Pathol 43:93‒96
Manimekalai R, VP Soumya, S Nair, GV
Thomas, VK Baranwal (2014b). Molecular characterization identifies 16SrXI-B
group phytoplasma ('Candidatus Phytoplasma
oryzae'-related strain) associated with root wilt disease of coconut in India. Sci Hortic 165:288‒294
Marcone C (2014). Molecular biology and
pathogenicity of phytoplasmas. Ann Appl
Biol 165:199‒221
Martinez RT, L Baudouin, A Berger, M
Dollet (2010). Characterization of the genetic diversity of the Tall coconut (Cocos nucifera L.) in the Dominican
Republic using microsatellite (SSR) markers. Tree Genet Genomics 6:73‒81
Martinez RT, M Narvaez, S Fabre, N
Harrison, C Oropeza, M Dollet, E Hichez (2008). Coconut lethal yellowing on the
southern coast of the Dominican Republic is associated with a new 16SrIV group
phytoplasma. Plant Pathol 57:366-366
Marzachì C (2004). Molecular diagnosis of
phytoplasmas. Phytopathol Med 43:228‒231
Mathen K, P Rajan, C Radhakrishnan Nair, M
Sasikala, M Gunasekharan, M Govindankutty, JJ Solomon (1990). Transmission of
root (wilt) disease to coconut seedlings through Stephanitis typica (Distant) (Heteroptera: Tingidae). Trop Agric 67:69‒73
Maust BE, F Espadas, C Talavera, M
Aguilar, JM Santamaría, C Oropeza (2003). Changes in carbohydrate metabolism in
coconut palms infected with the lethal yellowing phytoplasma. Phytopathology 93:976‒981
Mayer CJ, A Vilcinskas, J Gross (2011).
Chemically mediated multitrophic interactions in a plant-insect
vector-phytoplasma system compared with a partially nonvector species. Agric For Entomol 13:25‒35
Mazivele MOM, V Nuaila, M Durante, MM
Colombo, E Taviani (2018). Promising primers for detection of phytoplasma
causing coconut lethal yellowing disease in Mozambique. Phytoparasitica 46:301‒308
Mehdi A, VK Baranwal, M Kochu Babu, D
Praveena (2012). Sequence Analysis of 16S rRNA and secA Genes Confirms the
Association of 16SrI-B Subgroup Phytoplasma with Oil Palm (Elaeis guineensis Jacq.) Stunting Disease in India. J Phytopathol 160:6‒12
Mejía F, M Palmieri, C Oropeza, M Doyle, N
Harrison, E Aguilar, M Narváez, R Estrada, G Ortiz (2004). First report of
coconut lethal yellowing disease in Guatemala. Plant Pathol 53:800-800
Mittelberger C, L Obkircher, S Oettl, T
Oppedisano, F Pedrazzoli, B Panassiti, C Kerschbamer, G Anfora, K Janik (2017).
The insect vector Cacopsylla picta vertically transmits the bacterium ‘Candidatus phytoplasma mali’ to its progeny. Plant Pathol 66:1015‒1021
Mora-Aguillera G (2002). Dispersal
potential of lethal yellowing of the coconut palm. In: Proceedings of the
Expert Consultation on Sustainable Coconut Production through Control of Lethal
Yellowing Disease, Vol 18, pp:128‒130, Kingston, Jamica
Mpunami M, A Kullaya, J Mugini (2002). The
status of lethal yellowing-type diseases in East Africa. In: Proceedings of
the Expert Consultation on Sustainable Coconut Production through Control of
Lethal Yellowing Disease, Vol 18, pp:161‒168, Kingston, Jamica
Mpunami A, A Tymon, P Jones, MJ Dickinson
(2000). Identification of potential vectors of the coconut lethal disease
phytoplasma. Plant Pathol 49:355‒361
Mpunami AA, A Tymon, P Jones, MJ Dickinson
(1999). Genetic diversity in the coconut lethal yellowing disease phytoplasmas
of East Africa. Plant Pathol 48:109‒114
Mugini J (2002). Current status of coconut
lethal disease research in Tanzania. In: Proceedings
of the Expert Consultation on Sustainable Coconut Production through Control of
Lethal Yellowing Disease, CFC Technical Paper, Vol 18, pp:134‒142, Kingston, Jamica
Musetti R, P Ermacora, M Martini, N Loi, R
Osler (2013). What can we learn from the phenomenon of “recovery”? Phytopathog Mollic 3:63‒65
Myrie W, C Oropeza, L Sáenz, N Harrison,
MM Roca, I Córdova, S Ku, L Douglas (2011). Reliable improved molecular detection
of coconut lethal yellowing phytoplasma and reduction of associated disease
through field management strategies. Bull
Insectol 64:203‒204
Myrie W, N Harrison, M Dollet, B Been
(2007). Molecular detection and characterization of phytoplasmas associated
with lethal yellowing disease of coconut palms in Jamaica. Bull Insectol 60:159‒160
Myrie WA, L Douglas, NA Harrison, W
McLaughlin, M James (2012). First report of lethal yellowing disease associated
with subgroup 16SrIV, a phytoplasma on St. Kitts in the Lesser Antilles. New Dis Rep 26:25-25
Naderali N, N Nejat, G Vadamalai, RE
Davis, W Wei, NA Harrison, L Kong, J Kadir, YH Tan, Y Zhao (2017). ‘Candidatus Phytoplasma wodyetiae’, a new
taxon associated with yellow decline disease of foxtail palm (Wodyetia bifurcata) in Malaysia. Intl J Syst Ecol Microbiol 67:3765‒3772
Naderali N, G Vadamalai, N Nejat, KL Ling
(2015). First Report of Phytoplasma (16SrI) Associated with Yellow Decline
Disease of Royal Palms [Roystonea regia
(Kunth) O. F. Cook] in Malaysia. J
Phytopathol 163:133‒137
Naderali N, G Vadamalai, YH Tan, N Nejat
(2014). Detection and identification of aster yellows phytoplasma associated
with lipstick yellow frond disease in Malaysia. J Phytopathol 162:264‒268
Naderali N, N Nejat, YH Tan, G Vadamalai
(2013). First report of two distinct phytoplasma species, 'candidatus phytoplasma cynodontis' and 'candidatus phytoplasma asteris,' simultaneously associated with
yellow decline of Wodyetia bifurcata
(foxtail palm) in Malaysia. Plant Dis
97:1504-1504
Narvaez M, I Cordova, R Orellana, NA
Harrison, C Oropeza (2006). First report of a lethal yellowing phytoplasma in Thrinax radiata and Coccothrinax readii palms in the Yucatan Peninsula of Mexico. Plant Pathol 55:292-292
Narváez M, R Vázquez-Euán, NA Harrison, G
Nic-Matos, JF Julia, JL Dzido, S Fabre, M Dollet, C Oropeza (2018). Presence of
16SrIV phytoplasmas of subgroups A, D and E in planthopper Haplaxius crudus Van Duzee insects in Yucatán, Mexico. 3Biotech 8:61-70
Narvaez M, I Córdova-Lara, C
Reyes-Martínez, C Puch-Hau, L Mota-Narvaez, A Collí, G Caamal, N Harrison, L
Sáenz, C Oropeza (2016). Occurrence of 16SrIV Subgroup A Phytoplasmas in
Roystonea regia and Acrocomia mexicana Palms with Lethal Yellowing-like
Syndromes in Yucatán, Mexico. J
Phytopathol 164:1111‒1115
Nejat N, DM Cahill, G Vadamalai, M
Ziemann, J Rookes, N Naderali (2015). Transcriptomics-based analysis using
RNA-Seq of the coconut (Cocos nucifera)
leaf in response to yellow decline phytoplasma infection. Mol Genet Genomics 290:1899‒1910
Nejat N, G Vadamalai, RE Davis, NA
Harrison, K Sijam, M Dickinson, SNA Abdullah, Y Zhao (2013). 'Candidatus
phytoplasma malaysianum', a novel taxon associated with virescence and phyllody
of Madagascar periwinkle (Catharanthus
roseus). Intl J Syst Evol Micr 63:540‒548
Nejat N, K Sijam, SNA Abdullah, G
Vadamalai, M Dickinson (2009a). Molecular characterization of a phytoplasma
associated with Coconut Yellow Decline (CYD) in Malaysia. Amer J Appl Sci 6:1331‒1340
Nejat N, K Sijam, SNA Abdullah, G
Vadamalai, M Dickinson (2009b). Phytoplasmas associated with disease of coconut
in Malaysia: Phylogenetic groups and host plant species. Plant Pathol 58:1152‒1160
Nejat N, K Sijam, SNA Abdullah, G
Vadamalai, M Dickinson (2009c). First report of a 16SrXIV, 'Candidatus
Phytoplasma cynodontis' group phytoplasma associated with coconut yellow
decline in Malaysia. Plant Pathol 58:389-389
Nkansah-Poku J, R Philippe, RN Quaicoe, SK
Dery, A Ransford (2009). Cape Saint Paul Wilt Disease of coconut in Ghana: Surveillance
and management of disease spread. Oilseeds
Fats Crops Lipid 16:111‒115
Nkansah-Poku J, SK Dery, R Philippe
(2005). Reduction of spread of Cape St. Paul wilt disease (CSPWD) of coconut by
insecticidal hot-fogging and removal of diseased palms. Ghana J Agric Sci 38:193‒198
Ntushelo K, NA Harrison, ML Elliott
(2013). Palm Phytoplasmas in the Caribbean Basin. Palms 57:93‒100
Odewale JO, MN Okoye (2013). Bunch and nut
production of surviving coconut palms in lethal yellowing disease endemic area
of Nigeria. Intl J Plant Breed Gen 7:57‒64
Odewale JO, A Collines, CD Atago, G Odiowaya,
MJ Ahanor, AA Edokpayi, EO Uwadiae (2012). Comparison of yield and stability
assessment of five coconut (Cocos
nucifera L.) varieties in a lethal yellow disease (LYD) endemic field over
nine different environments. World J
Agric Sci 8:229‒233
Ogle L, H Harries (2005). Introducing the
vector: How coconut lethal yellowing disease may have reached the Caribbean. Ethnobot Res Appl 3:139‒142
Oliveira MJRA, S Castro, S Paltrinieri, A
Bertaccini, M Sottomayor, CS Santos, MW Vasconcelos, SMP Carvalho (2020).
“Flavescence dorée” impacts growth, productivity and ultrastructure of Vitis
vinifera plants in Portuguese “Vinhos Verdes” region. Sci Hortic 261:108742
Omar AF, A Alsohim, MR Rehan, KA
Al-Jamhan, E Pérez-López (2018). 16SrII phytoplasma associated with date palm
and Mexican fan palm in Saudi Arabia. Aust
Plant Dis Notes 13:39-45
Oppedisano T, B Panassiti, F Pedrazzoli, C
Mittelberger, PL Bianchedi, G Angeli, A De Cristofaro, K Janik, G Anfora, C
Ioriatti (2020). Importance of psyllids’ life stage in the epidemiology of
apple proliferation phytoplasma. J Pest
Sci 93:49‒61
Oropeza C, I Cordova, C Puch-Hau, R
Castillo, JL Chan, L Sáenz (2017). Detection of lethal yellowing phytoplasma in
coconut plantlets obtained through in
vitro germination of zygotic embryos from the seeds of infected palms. Ann Appl Biol 171:28‒36
Oshima K, S Kakizawa, H Nishigawa, HY
Jung, W Wei, S Suzuki, R Arashida, D Nakata, SI Miyata, M Ugaki, S Namba
(2004). Reductive evolution suggested from the complete genome sequence of a
plant-pathogenic phytoplasma. Nature Genet 36:27‒29
Osagie IJ, EE Ojomo, F Pilet (2015).
Occurrence of Awka wilt disease of coconut in Nigeria for one century. Phytopathog Mollic 5:61‒62
Ovasuru T (1994). The current status of
the coconut industry in Papua New Guinea. In: Coconut Improvement in the
South Pacific, pp:9‒13. Foale M, P Lynch (Eds.). ACIAR, Taveuni, Fiji
Pacifico D, L Galetto, M Rashidi, S Abbà,
S Palmano, G Firrao, D Bosco, C Marzachì (2015). Decreasing global transcript
levels over time suggest that phytoplasma cells enter stationary phase during
plant and insect colonization. Appl Environ
Microbiol 81:2591‒2602
Parakkunnel R, N Bindhani, S Purru, S
Lakhanpaul, K Venkataramanna Bhat (2020). Adaptive evolution and response to
phytoplasma: A genome-wide study of TCP transcription factors in Sesamum indicum L. Ann Appl Biol 176:75‒95
Parmesan C, G Yohe (2003). A globally
coherent fingerprint of climate change impacts across natural systems. Nature 421:37‒42
Perera L, MK Meegahakumbura, HRT
Wijesekara, WBS Fernando, J Dickinson (2012). A phytoplasma is associated with
the Weligama coconut leaf wilt disease in Sri Lanka. J Plant Pathol 94:205‒209
Pilet F, RN Quaicoe, IJ Osagie, M Freire,
X Foissac (2019). Multilocus sequence analysis reveals three distinct
populations of "Candidatus
Phytoplasma palmicola" with a specific geographical distribution on the
African continent. Appl Environ Microbiol
85:1-16
Pilet F, R Philippe, S Reignard, S
Descamps, R Quaicoe, J Nkansa-Poku, S Fabre, M Dollet (2009). Identification of
potential insect vectors of the Cape Saint Paul Wilt Disease of coconut in
Ghana by PCR. Oleag Corps Gras Lipid
16:107‒110
Pilotti CA, CF Dewhurst, LW Liefting, L
Kuniata, T Kakul (2014). Putative vectors of a phytoplasma associated with
coconut (Cocos nucifera) in Madang
Province, Papua New Guinea. Intl J Agric
For 4:365‒372
Quaglino F, F Sanna, A Moussa, M
Faccincani, A Passera, P Casati, PA Bianco, N Mori (2019). Identification and
ecology of alternative insect vectors of ‘Candidatus
Phytoplasma solani’ to grapevine. Sci Rep
9:1952-1963
Quaicoe RN, SK Dery, R Philippe, L
Baudouin, JO Nipah, J Nkansah-Poku, R Arthur, D Dare, YN Yankey, F Pilet, M
Dollet (2009). Resistance screening trials on coconut varieties to Cape Saint
Paul Wilt Disease in Ghana. Oilseeds Fats
Crops Lipid 16:132‒136
Queiroz RB, P Donkersley, FN Silva, IH
Al-Mahmmoli, AM Al-Sadi, CM Carvalho, SL Elliot (2016). Invasive mutualisms
between a plant pathogen and insect vectors in the Middle East and Brazil. Roy Soc Open Sci 3:1-12
Rajagopal V, KD Patil, B Sumathykuttyamma
(1986). Abnormal stomatal opening in coconut palms affected with root (wilt)
disease. J Exp Bot 37:1398‒1405
Rajan P (2013). Transmission of coconut
root (wilt) disease through plant hopper, Proutista moesta Westwood (Homoptera:
Derbidae). Pest Manage Hortic Ecosyst
17:1‒5
Ramjegathesh R, G Karthikeyan, D
Balachandar, K Ramaraju, L Rajendran, T Raguchander, R Samiyappan (2019).
Nested and TaqMan ® probe based quantitative PCR for the diagnosis of Ca.
Phytoplasma in coconut palms. Mol Biol
Rep 46:479‒488
Ramjegathesh R, G Karthikeyan, L
Rajendran, I Johnson, T Raguchander, R Samiyappan (2012). Root (wilt) disease
of coconut palms in South Asia - an overview. Arch Phytopathol Plant Prot 45:2485‒2493
Rashidi M, R D'Amelio, L Galetto, C
Marzachì, D Bosco (2014). Interactive transmission of two phytoplasmas by the
vector insect. Ann Appl Biol 165:404‒413
Roca MM, MG Castillo, NA Harrison, C
Oropeza (2006). First Report of a 16SrIV group phytoplasma associated with
declining coyol palms in honduras. Plant
Dis 90:526
Rosete YA, HATTA Diallo, JL Konan Konan,
AEP Kouamé, K Séka, KD Kra, MN Toualy, KE Kwadjo, WAMP Daramcoum, NI Beugré,
BWM Ouattara, CG Kouadjo Zaka, K Allou, ND Fursy-Rodelec, ON Doudjo-Ouattara, N
Yankey, S Dery, A Maharaj, M Saleh, R Summerbell, N Contaldo, S Paltrinieri, A
Bertaccini, J Scott (2016). Detection and identification of the coconut lethal
yellowing phytoplasma in weeds growing in coconut farms in Côte d’Ivoire. Can J Plant Pathol 38:164‒173
Santi S (2019). Laser microdissection of
phytoplasma-infected grapevine leaf phloem tissue for gene expression study. In:
Methods in Molecular Biology, pp:279‒290. Humana Press Inc., New
Jersey, USA
Serju C (2012). 30 years dedicated to
coconut cultivation. In: The Gleaner. The Gleaner Company, Kingston,
Jamaica
Seruga Musić M, HD Nguyen, S Cerni, Ð
Mamula, K Ohshima, D Skorić (2014). Multilocus sequence analysis of 'Candidatus Phytoplasma asteris' strain
and the genome analysis of Turnip mosaic virus co-infecting oilseed rape. J Appl Microbiol 117:774‒785
Singh RR, MH Ferguson (2017). First report
of a ‘Candidatus Phytoplasma
palmae’-related subgroup 16SrIV-D phytoplasma on Trachycarpus fortunei. Aust
Plant Dis Notes 12:1-3
Snaddon JL, KJ Willis, DW Macdonald
(2013). Biodiversity: Oil-palm replanting raises ecology issues. Nature 502:170‒171
Solomon JJ, V Hegde, M Babu, L Geetha
(2019). Phytoplasmal diseases. In: The Coconut Palm (Cocos nucifera L.) -
Research and Development Perspectives, pp:519‒556. Springer,
Singapore,
Stehle S, R Schulz (2015). Agricultural
insecticides threaten surface waters at the global scale. Proc Natl Acad Sci USA 112:5750‒5755
Sugio A, AM Maclean, SA Hogenhout (2014).
The small phytoplasma virulence effector SAP11 contains distinct domains
required for nuclear targeting and CIN-TCP binding and destabilization. New
Phytol 202:838‒848
Sunukumar SS, C Mohankumar, K Murugan
(2014). Purification and characterization of NADPH oxidase from Kerala wilt
disease coconut palm. Indo Amer J Pharm
Sci 4:2170‒2177
Tanno K, K Maejima, A Miyazaki, H Koinuma,
N Iwabuchi, Y Kitazawa, T Nijo, M Hashimoto, Y Yamaji, S Namba (2018).
Comprehensive screening of antimicrobials to control phytoplasma diseases using
an in vitro plant–phytoplasma
co-culture system. Microbiology 164:1048‒1058
Tedeschi R, A Bertaccini (2019).
Transovarial transmission in insect vectors. In: Phytoplasmas: Plant
Pathogenic Bacteria - II: Transmission and Management of Phytoplasma -
Associated Diseases, pp:115‒130. Springer, Singapore
Tedeschi R, V Ferrato, J Rossi, A Alma
(2006). Possible phytoplasma transovarial transmission in the psyllids Cacopsylla melanoneura and Cacopsylla pruni. Plant Pathol 55:18‒24
Thuiller W (2007). Biodiversity: Climate
change and the ecologist. Nature 448:550‒552
Tymon AM, P Jones, NA Harrison (1998).
Phylogenetic relationships of coconut phytoplasmas and the development of
specific oligonucleotide PCR primers. Ann
Appl Biol 132:437‒452
Valiunas D, R Jomantiene, A Ivanauskas, D
Sneideris, M Zizyte-Eidetiene, J Shao, Z Yan, S Costanzo, RE Davis (2019).
Rapid detection and identification of ‘Candidatus
phytoplasma pini’-related strains
based on genomic markers present in 16S rRNA and tuf genes. For Pathol 49;
Article 12553
Vázquez-Euán R, N Harrison, M Narvaez, C
Oropeza (2011). Occurrence of a 16SrIV group phytoplasma not previously
associated with palm species in Yucatan, Mexico. Plant Dis 95:256‒262
Wang Z, Y Zhu, Z Li, X Yang, T Zhang, G
Zhou (2020). Development of a Specific Polymerase Chain Reaction System for the
Detection of Rice Orange Leaf Phytoplasma Detection. Plant Dis 104:521‒526
Warokka JWJ, PJP Jones, MDM Dickinson
(2006). Detection of phytoplasmas associated with Kalimantan wilt disease of
coconut by the polymerase chain reaction. J
Penelit Tanam Indust 12:154‒160
Wei
W, RE Davis, GR Bauchan, Y Zhao (2019). New symptoms identified in
phytoplasma-infected plants reveal extra stages of pathogen-induced meristem
fate-derailment. Mol Plant-Microb
Interact 32:1314‒1323
Wei W, RE Davis, IM Lee, Y Zhao (2007).
Computer-simulated RFLP analysis of 16S rRNA genes: Identification of ten new
phytoplasma groups. Int J Syst Ecol Microbiol
57:1855‒1867
Weintraub PG, L Beanland (2006). Insect
vectors of phytoplasmas. Annu Rev Entomol 51:91‒111
Weintraub PG, V Trivellone, K Krüger
(2019). The biology and ecology of leafhopper transmission of phytoplasmas. In:
Phytoplasmas: Plant Pathogenic Bacteria - II: Transmission and Management of
Phytoplasma - Associated Diseases, pp:27‒51. Springer, Singapore
Yadav V, S Mahadevakumar, GR Janardhana, C
Amruthavalli, MY Sreenivasa (2015). Molecular detection of 'Candidatus phytoplasma trifolii'
associated with little leaf of brinjal from Kerala state of Southern India. Intl J Life Sci 9:109‒112
Zamharir MG, MR Eslahi (2019). Molecular
study of two distinct phytoplasma species associated with streak yellows of
date palm in Iran. J Phytopathol 167:19‒25
Zamharir MG, SMS Boshehri, Y Khajehzadeh
(2016). Candidatus phytoplasma
fraxini related (16S rRNAVII) strain associated with date yellows disease in
Iran. Aust Plant Dis Notes 11:31-34
Zimmermann MR, T Knauer, ACU Furch (2019). Collection of
phloem sap in phytoplasma-infected plants. In: Methods in Molecular Biology,
pp:291‒299. Humana Press Inc., New Jersey, USA