Anthracnose, caused by Colletotrichumtheae sinensis, is
one of the most severe diseases that can afflict many crops such as pepper,
grape, and tea, etc. (Liu et al. 2015;
Wang
et al. 2016; Waskow et
al. 2016, Mishra et al. 2017). The disease could attack any parts of a plant at any
growth stage. It causes leaf spots, blotches, defoliation, twig cankers and
dieback on many different plants. The disease can decrease the plant's vigor,
weakening the plant growth and decreasing the quality and yield of the host
crop (Chowdhury and Rahim 2009; Ali et al. 2014; Cota et al. 2017).
Photosynthesis plays an important
role in plant
disease defense responses (Dong et al. 2016). In general, disease has a strong negative
influence on plant photosynthesis (Prokopová et
al. 2010; Zhao et al. 2011; Hu et al. 2018), while resistance to disease has a positive
influence on plant photosynthesis. The highly
disease-resistant cultivar usually exhibits a high rate of photosynthesis and
may obtain high yields in regions of widespread disease. In, Hu et al. 2018 found that bacterial leaf blight infection had a
higher maximal photosynthetic rate and dark respiration rate in resistant rice
than in susceptible one. Debona et al. (2014)
also reported that, for two wheat cultivars infected with Pyricularia oryzae, the susceptible cultivar (BR 18)
exhibited a drastically reduced net photosynthesis rate compared with the
partially resistant cultivar.
Chlorophyll
(Chl) fluorescence, which is released in plant photosynthesis, is a rapid,
non-destructive detection method for abiotic and biotic stress in plants. In 2002, Bassanezi et al. found that the minimal fluorescence (F0) was remarkably reduced in bean leaves after
infection by an angular leaf spot. Zhori et al.
(2015) also reported that the rapid fluorescence kinetics was used in situ in the field to monitor the
healthy and Uromyces-infected plants of Euphorbia
cyparissias. It proved to be
useful for differentiating between the infected and healthy plants and may be
used in the investigation on the disease severity.
Tea plants have been widely cultivated in most areas and
tea is considered an important beverage around the world (Paiano et
al. 2014). The fungicide and pesticide residues greatly affect the quality
of raw tea products and may pose many risks to consumer’s health (Jaggi et
al. 2001; Gupta et al. 2008). Photosynthesis related to tea plant growth plays an
important role in disease defense management. There is a close relationship
between plant photosynthesis and leaf chlorophyll status. The disease may
affect the photosynthesis by destroying the
chlorophyll. Limited information has been reported on the effect of
anthracnose disease on the photosynthetic characteristics and the related
chlorophyll changes of tea plants. Monitoring of tea anthracnose incidence based on photosynthesis using Chl
fluorescence has also seldom been reported. It is known
that planting resistant varieties is an efficient, reliable, and cheap way to
manage disease (Silva et al. 2018); however, the effects of the disease
resistance on tea plant photosynthesis have not been reported.
This study aims to research the
leaf photosynthetic rate and the Chl fluorescence parameters which may be involved in these
changes after the tea plant was infected by anthracnose. It was hypothesized
that photosynthetic rate is damaged by anthracnose infection and the damage may
differ between resistant and susceptible cultivars. Moreover, the reduction in
photosynthesis may be related to stomata closure and decreased pigment.
To evaluate these hypotheses, anthracnose disease severity, photosynthetic
traits, and feasibility of some Chl fluorescence parameters which may be used to monitor the anthracnose disease was
discussed in two tea cultivars with variable resistance to anthracnose.
Glasshouse experiments were conducted at the Zhejiang Academy of
Agricultural Sciences (ZAAS), Zhejiang province, P.R. China in the 2017 growing
season. Two-year seedlings of anthracnose susceptible and resistant tea plants Longjing 43 and Yingshuang were
planted in 30 L polyvinyl chloride pots (one plant each pot) in the glasshouse.
The physical and chemical properties of the cultivated soil were N content
0.835 g.kg-1, pH 6.21, organic matter content 13.63 g.kg-1,
available phosphorus and potassium 25.28 and 49.66 g.kg-1.
The experiment consisted of four treatments that are healthy (CK), slight
(D1), moderate (D2) and serious (D3) disease grade. Each
treatment had seven tea plants. The trial was set up as a completely randomized
block arrangement with three replications. Anthracnose inoculations were
performed manually. The youngest fully expanded leaves (the second or third
leaf from the top) were selected and inoculated by a hypodermic syringe needle
method on June 15, 2017, and CK was inoculated in deionized water. The anthracnose
infected treatments D1, D2, D3 were created and inoculated in 105,
106 and 107 conidia/mL anthracnose suspension. Inoculated
and control plants were seal-covered with polyvinyl chloride and maintained at
25°C and 90% relative air humidity with a 12-h
photoperiod for 5 days. Disease incidence, leaf photosynthesis rate and Chl fluorescence were measured at 30 days after
inoculation.
Three plants of each variety were selected to assess disease incidence on
the leaves. According to visual observations, the disease severity degree was
measured by a 5 grade scale based on the percent area of leaf affected (0, 1–10%,
11–25%, 26–50%, 51–75% and above 75%). The percent disease index (PDI) was
calculated by the method of Sridhar and Sohi (1970).
where S represents the sum of numerical leaves, T represents the total number of leaves, and M represents the maximum disease scale.
The net photosynthesis rate (Pn), transpiration rate (Tr),
stomatal conductance (Gs) and
intercellular carbon dioxide concentration (Ci)
in leaves were measured and recorded on fully developed clean leaf using a
portable photosynthesis system (Ciras-II, PP Systems,
UK). The photosynthetic chamber with irradiance levels of 1000 μmol m-2 s-1 provided a leaf
area of 1.7 cm2, relative air humidity of 70%, and a CO2
concentration of 400 μmol mol-1.
Transient Chl
fluorescence (OJIP) was measured using Multi-Function Plant Efficiency Analyser (Hansatech, UK) after
the leaves adapted to the dark for about 30 min. A fluorescence intensity recorded at 20 μs, 2 ms, 30 ms and the maximum represented the O, J, I and P point. The biophysical parameters, such as
absorption, trapping, electron transport, and dissipation per active reaction
center (ABS/RC, TR0/RC, ET0/RC,
DI0/RC), were calculated from the obtained data.
The
tea plant leaves were measured by the Chl
fluorometer imaging system (Open FluorCam,
Photon Systems Instruments, Brno, Czech Republic) after they adapted to the dark. In this system, a charge-coupled device camera was
used, which produces a
pseudo-color 512×512 pixel fluorescence images.
The imaging fluorometer was controlled and the images were analyzed by the FluorCam software (Photon Systems Instruments, Brno, Czech
Republic). The minimum fluorescence (F0),
maximal fluorescence (Fm), the
maximum quantum
efficiency of PSII (Fv/Fm),
the effective photochemical quantum yield of PSII (ΦPSII), and non-photochemical quenching (NPQ) were auto measured and stored in the computer. The above
fluorescence parameter images were shown randomly and the mean of all
fluorescence values was given.
Table
1: Percent disease index
(PDI) of CK, D1, D2 and D3 treatments in Longjing 43 and
Yingshuang tea plants
Treatment |
Longjing 43 |
Yingshuang |
CK |
0d |
0d |
D1 |
8.55c |
4.32c |
D2 |
21.33b |
8.18b |
D3 |
43.69a |
13.57a |
Note: CK,
D1, D2 and D3 represent healthy, slight, moderate and
serious anthracnose disease treatments. Mean values for various
treatments followed by the same letter are not significantly different
(P<0.05) according to the LSD test. CK was inoculated with deionized water.
D1, D2 and D3 were inoculated with 105, 106 and 107 conidia/ml
anthracnose suspension, the same as below
Table
2: Pigment contents of CK, D1, D2 and D3 treatments in Longjing
43 and Yingshuang tea plants
Cultivar |
Treatment |
Chl a |
Chl b |
Car |
Chl a+Chl b |
CK |
2.62a |
0.87a |
1.21a |
3.50a |
|
Longjing 43 |
D1 |
2.00b |
0.64b |
1.13b |
2.64b |
D2 |
1.63c |
0.51c |
1.07c |
2.13c |
|
D3 |
1.70c |
0.64b |
1.08c |
2.34bc |
|
CK |
2.65a |
0.87a |
1.16 |
3.52a |
|
Yinshuang |
D1 |
1.94b |
0.46b |
1.09 |
2.40b |
D2 |
1.58bc |
0.41b |
1.09 |
1.99b |
|
D3 |
1.48c |
0.50b |
1.03 |
1.98b |
Note: Chl a, Chl b and Car represent chlorophyll a, chlorophyll b and
carotenoid content
The pigment content in the leaf was collected with 80% acetone. Absorption
at 663, 645 and 470 nm was measured using an ultraviolet-visible (UV)
spectrophotometer (Unico, UV-3802, China). Chl a, Chl b and carotenoid (Car)
content were calculated as previously described (Arnon 1949). The unit of the photosynthesis
pigment content was mg.g-1 based on fresh mass.
Data analyses were performed by SPSS 17.0 (SPSS Inc., Chicago, USA). Differences
in parameters within various treatments (CK, D1, D2, and D3) were assessed with
one-way analysis of variance with multiple comparisons of means using Fisher's
LSD test at the 0.05 level. All of the measurements were performed three times,
and calculated standard errors (SE) were reported.
PDI of healthy and anthracnose infected plants of Longjing
43 and Yingshuang was shown in Table 1. In Longjing 43, PDI increased almost linearly during
evaluation treatments, ranging on average from 8.55 in D1 to 43.69 in D3.
Compared with Longjing 43, Yingshuang
had smaller fleck symptoms with PDI 4.32, 8.18 and 13.57 in D low, D med and D sev anthracnose infected treatment. Across the two tea
plants, significant differences in PDI were found among all the treatments and
PDI increased significantly with the anthracnose development. Comparably, Yingshuang had lower PDI than Longjing
43 when they were infected by anthracnose disease.
The pigment of Longjing 43 and Yingshuang following infection by anthracnose is shown in
Table 2. Compared with the healthy plants (CK), the total of Chl a
and Chl b
content reduced 32.3 and 39.6% in anthracnose infected Longjing
43 and Yingshuang. Significant differences in Chl a, Chl b and the total of Chl a
and Chl b in Longjing
43 and Yingshuang between CK and D1 or D2 treatments
were found. There were no significant differences between D2 and D3 treatments
for Chl a and Chl a+Chl b across the two tea plants. The statistically
significant difference in Car between
CK and the infected treatments in Longjing 43 was
observed.
Fig. 1: Changes of net
photosynthesis rate (Pn).
(A): transpiration rate (Tr);
(B): stomatal conductance (Gs); (C): intercellular carbon
dioxide concentration (Ci);
(D) CK, D1, D2 and D3 treatments in Longjing 43 and Yingshuang tea plants
Note: CK, D1, D2 and D3 represent healthy, slight, moderate and serious
anthracnose disease treatments, respectively. Mean values for various
treatments followed by the same letter are not significantly different (P< 0.05) according to the LSD test.
CK was inoculated with deionized water. D1, D2 and D3 were inoculated with 105,
106 and 107 conidia/ml anthracnose suspension. The means
and calculated standard errors are reported, the same as below
Fig. 2: Chlorophyll fluorescence OJIP
transient curves of CK, D1, D2 and D3 treatments in Longjing
43 (A) and Yingshuang (B) tea plants
Fig. 1 shows the changes of Pn, Tr,
Gs and Ci of CK, D1, D2 and D3 treatments in Longjing43 and Yingshuang plants. Compared with healthy plants (CK), Pn, Gs in the two
anthracnose infected tea plants decreased significantly. Pn in anthracnose
infected Longjing 43 and Yingshuang
decreased 73.8 and 53.8% in comparison with healthy plants. On the whole, Longjing 43 had low Pn than Yingshuang. With the
development of anthracnose infection, Tr in longjing43
deceased gradually. No significant changes for Ci in Longjing 43 and Yingshuang
were found after infection with anthracnose disease.
Fig. 2 (A, B) shows that the differences in transient Chl fluorescence
existed between CK, D1, D2 and D3 treatments for Longjing
43 and Yingshuang tea plants. It revealed
characteristic fluorescence transient curve shape (OJIP curve) with differences
in healthy and anthracnose-infected tea plants. Collectively, there was lower Chl fluorescence in anthracnose-infected treatments (D1,
D2 and D3) compared to CK across the two tea plants. Among the treatments, small
differences in O point and great
differences in P point were observed.
The differences in J, I, P
points in the OIJP curves increased gradually from CK to D3 treatments.
Fig. 3 (A, B) shows the parameters indicating
the absorption (ABS/RC), trapping (TRo/RC), electron transport (ETo/RC) and dissipation (DIo/RC) per reaction center of PSII
calculated from the fluorescence transient curve in
Fig. 3: Energy pipeline
models of specific fluxes per reaction center (RC) of CK, D1, D2 and D3
treatments in Longjing 43 (A) and Yingshuang
(B) tea plants. ABS/RC, TR0/RC, ET0/RC and DI0/RC
indicate absorption, trapping, electron transport and dissipation per active RC
Fig. 4: Changes in chlorophyll fluorescence
parameters F0, Fm, Fv/Fm,
ΦPSII and NPQ images of CK, D1, D2 and D3
treatments in Longjing43 (A) and Yingshuang (B) tea
plants. F0, Fm, Fv/Fm,
ΦPSII and NPQ indicate the minimum fluorescence,
maximal fluorescence, maximum quantum efficiency of PSII, effective
photochemical quantum yield of PSII, and non-photochemical quenching
CK, D1, D2, and D3 treatments in Longjing 43 and Yingshuang
plants. Collectively, ABS/RC,
DIo/RC, ETo/RC, TRo/RC increased after infection by
anthracnose across the two tea plants. Comparably, the differences in
the above parameters between CK and D1 were smaller than CK with D2 and D3
treatments.
Chlorophyll a fluorescence image
Dark and light adapted Chl fluorescence parameters F0, Fm, Fv/Fm, ΦPSII,
and NPQ of CK, D1, D2, D3 treatments
in Longjing 43 and Yingshuang
are shown in Fig. 4. The average values of the above parameters are shown in
Table 3. Across the two tea plants, the reductions of Fm, Fv/Fm
and ΦPSII in infected
treatments in comparison with CK were observed. F0 in Longjing 43 decreased
significantly after infection by anthracnose. No significant difference in F0 between CK and the
infected treatments in Yingshuang plants, while NPQ reached the maximum in D1, while the
transition from D1 to D3 exhibited a decrease.
To date, the study of tea plant disease has been concentrated on the
chemical composition and the quality of tea affected by the disease and disease
control (Gulati et
al. 1999; Sanjay et al. 2008; Pallavi
et al. 2012). The effects of disease infection on photosynthetic
characteristics in tea plants were closely related to the quality and quantity
of tea production (Gulati et al. 1999).
To our knowledge, this is the first time that the impact of anthracnose infection
on tea leaf photosynthesis has been reported. Tea leaves were damaged gradually as the anthracnose
disease developed. In the experiments presented here, anthracnose caused PDI
values of 13.57 in Yingshuang and 43.69 in Longjing 43. This suggested that Yingshuang
was highly resistant to anthracnose infection while Longjing
43 was susceptible.
Table 3: Chlorophyll
fluorescence parameters F0,
Fm,
Fv/Fm,
ΦPSII and NPQ of CK, D1, D2 and D3 treatments in Longjing 43 and Yingshuang tea
plants
Cultivar |
Treatment |
F0 |
Fm |
Fv/Fm |
ΦPSII |
NPQ |
Longjing 43 |
CK |
274.2a |
1281.8a |
0.78a |
0.60a |
0.63b |
D1 |
265.63a |
1171.8a |
0.77a |
0.57ab |
0.72a |
|
D2 |
241.36b |
865.7b |
0.70b |
0.51bc |
0.61b |
|
D3 |
214.89c |
703.8c |
0.68b |
0.48c |
0.39c |
|
Yingshuang |
CK |
296.4 |
1542.4a |
0.81a |
0.61a |
0.56a |
D1 |
303.1 |
1391.9b |
0.78ab |
0.58a |
0.57a |
|
D2 |
293.4 |
958.5c |
0.68bc |
0.43b |
0.61a |
|
D3 |
253.8 |
750.6d |
0.64c |
0.45b |
0.40b |
Note: F0, Fm, Fv/Fm,
ΦPSII, NPQ indicate the minimum fluorescence,
maximal fluorescence, maximum quantum efficiency of PSII, effective
photochemical quantum yield of PSII, and non-photochemical quenching
Pigments are important parts of plant
photosynthesis. Reduction of Chl a, Chl b and Car
was observed after the two tea plants infected by anthracnose disease in the
experiment. The result was similar to the report by Lobato et al. (2010). Scarpari et
al. (2005) also found that Chl a and Chl b reduced in Theobroma cacao plants infected by the pathogen Crinipellis perniciosa.
The significantly decreased amount of Chls in
anthracnose infected plants may be due to decreased leaf photosynthetic area
promoting less light absorption, and chloroplast damages during disease
infection (Radwan et al. 2008).
Limited photosynthesis was observed in two tea
varieties after anthracnose infection, and Chls and stomatal
conductance may be considered to explain. Decreased Chls
may cause the depressed photosynthesis rate as mentioned above due to the close
relationship between photosynthesis and Chls. A lower
Gs
is one of the major constraints to photosynthesis in disease infected plants by
limiting CO2 influx into leaves (Erickson et al. 2003). Gs were greater in healthy plants and decreased with increased
disease severity. The lower Gs in tea
plants resulted in lower Tr. da Silva
et al. (2018) also reported that a
partial closure of the stomata results in the reduction of photosynthesis and
the transpiration rate in eucalyptus plants after infection with Ceratocystis fimbriata. Interestingly,
almost no great changes were found in Ci in
the two tea plants with the development of anthracnose disease, suggesting that
the reduction of Chls
was the main factor for the impaired photosynthesis in tea plants caused by the
anthracnose infection.
The transient OJIP indicates the response of plants to environmental
stress. Disease stress could change the special sites of the transient OJIP and
reduce fluorescence intensity at the J,
I, and P steps (Baker 2008). In our experiment,
higher Chl
fluorescence values in healthy plants than anthracnose infected ones were found
in two tea plants. There were great differences in P point and the differences at the J, I and P point in the OIJP curves increased
gradually with the development of anthracnose disease. The decreased P point caused by anthracnose in the
OIJP test provided an explanation for the reduction of Fv/Fm in the Chl fluorescence images. Some
parameter values in D1 treatments were similar or even lower than healthy ones.
It may be related to the response of the plant itself to the disease.
Electron transport is the first stage of
photosynthesis that produces chemical energy (Trebst
2003). It may mainly occur in PSII and some electron transport parameters such
as ABS/RC, TR0/RC,
ET0/RC and DI0/RC indicating the activity of PSII reaction center were analyzed. In
general, damage to PSII RCs under anthracnose disease was observed in this
study. Almost all the ABS/RC, DI0/RC, TR0/RC, and ET0/RC
in infected treatments were higher than those in healthy plants. These results
suggested that PSII RCs may be inactive and the efficiency per RC may be enhanced
during the electron transport process. Compared with the other parameters, a
sharp increase in DI0/RC
was observed. It indicated that most energies in RC dissipated in a form of heat due to
self-protection when a plant was in disease conditions (Monneveux et al. 2003). Interestingly, the ABS/RC, DI0/RC,
TR0/RC and ET0/RC of Longjing
43 in D1 (slight disease) were lower than or even similar to those in healthy
plants at the first stage of the infection treatment and reached the maximum in
D2. While in Yingshuang, those parameters ET0/RC increased and reached
the maximum in D3, suggesting that Longjing 43 might
be more susceptible infected from anthracnose disease than in Yingshuang. to maintain growth by
inhibiting electron transport and decreasing PSII photochemical activity during
the earlier stage of the disease stress.
The anthracnose infection induced decreased Fm, Fv/Fm, ΦPSII across the resistant and sensitive tea plants. It
suggested that these parameters have
the potential to be used to differentiate and monitor the anthracnose disease
in the application. On the parameter F0,
Bassanezi et al. (2002) found that the value remarkably
reduced in bean leaves after infection by an angular leaf spot. In our
experiment, the decreased F0
was observed in susceptible Longjing 43 after
infection by anthracnose, but not in resistant Yingshuang. This result showed that anthracnose resistance of tea plants had a
significant effect on F0.
, On Fv/Fm,
Tung et al. (2013) reported that the parameters Fv/Fm would be appropriate for
the detection of foliar plant infections. But some researchers found that Fv/Fm value did not change in Eupatorium makinoi
infected by geminivirus (Funayama
et al. 1997) but was significantly
lower in Nicotiana tabacum (Ryšlavŕ et al. 2003), and in Oncidium (Chia and He 1999) after
virus infection. On ФPSII,
Brabandt et al.
(2014) found that ФPSII
proved to be appropriate for early and objective detection of susceptible
butterhead lettuce eight days after inoculation under laboratory conditions.
Whether the above parameters could be appropriate for objective detection of
the other disease infection, need to be researched further.
Conclusion
Anthracnose decreased photosynthesis in leaves of
susceptible and resistant tea plants mainly by the reduced Chls. The electron transport
chain and PSII photochemical activity were inhibited after tea plants were
infected by anthracnose. The OJIP curves and the parameters Fm, Fv/Fm,
and ΦPSII might be
used to differentiate and monitor the anthracnose disease. The result of this
study might contribute to the knowledge of the disease’s effect on
photosynthesis in the leaves of tea plants and provide a valuable application
for disease monitoring.
Acknowledgments
This research was
supported by the Public Projects of Zhejiang Province, China (No. LGN18C140005) and the National Natural Science Foundation of China
(No. 31501220, 41601024). Thanks are given to the Beijing EcoTech Company for providing the portable chlorophyll
fluorometer (FluorCam).
Author Contributions
Hao Hu, Mei-Jun Tang and Yu-Wei Yuan conceived of the presented idea. Hua-Wei
Guo, Guang-Zhi Zhang, Qing Gu, Li Sheng, Hong-Kui Zhou, Zhi
Liu performed the experiment. Hao Hu wrote the original manuscript and all
authors discussed the results and contributed to the final manuscript.
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