Introduction

 

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.

 

Materials and Methods

 

Plant materials

 

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.

 

Experimental design and inoculation

 

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.

 

Percent disease index

 

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.

 

Leaf Gas exchange measurement

 

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.

 

Chlorophyll fluorescence transient measurements

 

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.

 

Chlorophyll fluorescence imaging system

 

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.

 

Pigment contents

 

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

 

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.

 

Results

 

Percent disease index

 

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.

 

Pigment contents

 

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.

 

Leaf gas exchange

 

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.

 

Chlorophyll fluorescence transient

 

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.

 

Discussion

 

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.

 

References

 

Ali A, WL Chow, N Zahid, MK Ong (2014) Efficacy of propolis and cinnamon oil coating in controlling post-harvest anthracnose and quality of chilli (Capsicum annuum L.) during cold storage. Food Bioprocess Technol 7:2742‒2748

Arnon DI (1949) Copper enzymes in isolated chloroplasts: Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1‒15

Baker NR (2008) Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89‒113

Bassanezi RB, L Amorim, RD Berger (2002) Gas exchange and emission of chlorophyll fluorescence during the monocycle of rust, angular leaf spot and anthracnose on bean leaves as a function of their trophic characteristics. J Phytopathol 150:37‒47

Brabandt H, E Bauriegel, U Gaerber, WB Herppich (2014) ФPSII and NPQ to evaluate Bremia lactucae-infection in susceptible and resistant lettuce cultivars. Sci Hortic 180:123‒129

Chia TF, J He (1999) Photosynthesic capacity in Oncidium (Orchidacceae) plants after virus eradication. Environ Exp Bot 42:11‒16

Chowdhury MNA, MA Rahim (2009) Integrated crop management to control anthracnose (Colletotrichum gloeosporioides) of mango. J Agric Rural Dev Trop 7:115‒120

Cota LV, AGC Souza, RV Costa, DD Silva, FE Lanza, FM Aguiar, JEF Figueiredo (2017) Quantification of yield losses caused by leaf anthracnose on sorghum in Brazil. J Phytopathol 165:479‒485

da Silva AC, FM de Oliveira Silva, JC Milagre, RP Omena-Garcia, MC Abreu, RG Mafia, A Nunes-Nesi, AC Alfenas (2018) Eucalypt plants are physiologically and metabolically affected by infection with ceratocystis fimbriata. Plant Physiol Biochem 123:170‒179

Debona D, FÁ Rodrigues, JA Rios, SC Martins, LF Pereira, FM DaMatta (2014) Limitations to photosynthesis in leaves of wheat plants infected by Pyricularia oryzae. Phytopathology 104:34‒39

Dong X, M Wang, N Ling, QR Shen, SW Guo (2016) Potential role of photosynthesis-related factors in banana metabolism and defense against Fusarium oxysporum f. sp. cubense. Environ Exp Bot 129:4‒12

Erickson JE, GR Stanosz, EL Kruger (2003) Photosynthetic consequences of Marssonina leaf spot differ between two poplar hybrids. New Phytol 161:577‒583

Funayama S, K Sonoike, I Terashima (1997) Photosynthetic properties of leaves of Eupatorium makinoi infected by a geminivirus. Photosyn Res 52:253‒261

Gulati A, A Gulati, SD Ravindranath, AK Gupta (1999) Variation in chemical composition and quality of tea (Camellia sinensis) with increasing blister blight (Exobasidium vexans) severity. Mycol Res 103:1380‒1384

Gupta M, A Sharma, A Shanker (2008) Dissipation of imidacloprid in orthodox tea and its transfer from made tea to infusion. Food Chem 106:158‒164

Hu H, L Sheng, GZ Zhang Q Gu, KF Zheng (2018) Influence of bacterial leaf blight on the photosynthetic characteristics of resistant and susceptible rice. J Phytopathol 166:547‒554

Jaggi S, C Sood, V Kumar, SD Ravindranath, A Shanker (2001) Leaching of pesticides in tea brew. J Agric Food Chem 49:5479‒5483

Liu F, BS Weir, U Damm, PW Crous, Y Wang, B Liu, M Wang, M Zhang, L Cai (2015) Unravelling Colletotrichum species associated with Camellia: Employing ApMat and GS loci to resolve species in the C. gloeosporioides complex. Persoonia 35:63‒84

Lobato AKS, MC Gonçalves-Vidigal, PS Vidigal Filho, CAB Andrade, MV Kvitschal, CM Bonato (2010) Relationships between leaf pigments and photosynthesis in common bean plants infected by anthracnose. New Zeal J Crop Hortic 38:9‒37

Mishra R, S Nanda, E Rout, SK Chand, JN Mohanty, RK Joshi (2017) Differential expression of defense-related genes in chilli pepper infected with anthracnose pathogen Colletotrichum truncatum. Physiol Mol Plant Pathol 97:1‒10

Monneveux P, C Pastenes, MP Reynolds (2003) Limitations to photosynthesis under light and heat stress in three high-yielding wheat genotypes. J Plant Physiol 160:657‒666

Paiano V, G Bianchi, E Davoli, E Negri, R Fanelli, E Fattore (2014) Risk assessment for the Italian population of acetaldehyde in alcoholic and non-alcoholic beverages. Food Chem 154:26‒31

Pallavi RV, P Nepolean, A Balamurugan, R Jayanthi, T Beulah, R Premkumar (2012) In vitro studies of biocontrol agents and fungicides tolerance against grey blight disease in tea. Asian Pac J Trop Biomed 2:S435‒S438

Prokopová J, M Špundová, M Sedlářová, A Husičková, R Novotný, K Doležal, J Naus, A Lebeda (2010) Photosynthetic responses of lettuce to downy mildew infection and cytokinin treatment. Plant Physiol Biochem 48:716‒723

Radwan DEM, G Lu, KA Fayez, SY Mahmoud (2008) Protective action of salicylic acid against bean yellow mosaic virus infection in Vicia faba leaves. J Plant Physiol 165:845‒857

Ryšlavŕ H, K MÜller Š Semorŕdovŕ, H Synkovŕ, N Čerovskŕ (2003) Photosynthesis and activity of phosphoenolpyruvate carboxylase in Nicotiana tabacum L. leaves infected by potato virus A and potato virus Y. Photosynthetica 41:357‒363

Sanjay R, P Ponmurugan, UI Baby (2008) Evaluation of fungicides and biocontrol agents against grey blight disease of tea in the field. Crop Prot 27:689‒694

Scarpari LM, LW Meinhardt, P Mazzafera, AWV Pomella, M Schiavinato, AJCM Cascardo, GAG Pereira (2005) Biochemical changes during the development of witches' broom: the most important disease of cocoa in Brazil caused by Crinipellis perniciosa. J Exp Bot 56:865‒877

Silva MS, FBM Arraes, MA Campos, M Grossi-de-Sa, D Fernandez, ES Cândido, MH Cardoso, OL Franco, MF Grossi-de-Sa (2018) Review: Potential biotechnological assets related to plant immunity modulation applicable in engineering disease-resistant crops, Plant Sci 270:72‒84

Sridhar TS, HS Sohi (1970) Relative resistance and susceptibility of different grape varieties against Gloeosporium ampelophagum Sacc. Ind J Hortic 27:161‒164

Trebst A (2003) Energy conservation in photosynthetic electron transport of chloroplasts. Annu Rev Plant Biol 25:423‒458

Tung J, PH Goodwin, T Hsiang (2013) Chlorophyll fluorescence for quantification of fungal foliar infection and assessment of the effectiveness of an induced systemic resistance activator. Eur J Plant Pathol 136:301‒315

Wang YC, XY Hao, L Wang, B Xiao, XC Wang, YJ Yang (2016) Diverse Colletotrichum species cause anthracnose of tea plants (Camellia sinensis (L.) O. Kuntze) in China. Sci Rep 6; Article 35287

Waskow B, RA Mano, RX Giacomini, DH Oliveira, RF Schumacher, EA Wilhelm, C Luchese, L Savegnago, RG Jacob (2016) Synthesis and Beckmann rearrangement of novel (Z)-2-organylselanyl ketoximes: Promising agents against grapevine anthracnose infection. Tetrahedron Lett 57:5575‒5580

Zhao D, NC Glynn, B Glaz, JC Comstock, S Sood (2011) Orange rust effects on leaf photosynthesis and related characters of sugarcane. Plant Dis 95:640‒647

Zhori A, M Meco, H Brandl, R Bachofen (2015) In situ chlorophyll fluorescence kinetics as a tool to quantify effects on photosynthesis in Euphorbia cyparissias by a parasitic infection of the rust fungus Uromyces pisi. BMC Res Notes 8; Article 698