Browse > Article
http://dx.doi.org/10.5423/PPJ.OA.09.2018.0180

Hydrogen Peroxide Prompted Lignification Affects Pathogenicity of Hemi-biotrophic Pathogen Bipolaris sorokiniana to Wheat  

Poudel, Ajit (Institute of Agricultural Sciences, Banaras Hindu University)
Navathe, Sudhir (Institute of Agricultural Sciences, Banaras Hindu University)
Chand, Ramesh (Institute of Agricultural Sciences, Banaras Hindu University)
Mishra, Vinod K. (Institute of Agricultural Sciences, Banaras Hindu University)
Singh, Pawan K. (International Maize and Wheat Improvement Center (CIMMYT))
Joshi, Arun K. (Borlaug Institute for South Asia (BISA))
Publication Information
The Plant Pathology Journal / v.35, no.4, 2019 , pp. 287-300 More about this Journal
Abstract
Spot blotch caused by Bipolaris sorokiniana has spread to more than 9 million ha of wheat in the warm, humid areas of the Eastern Gangetic Plains (EGP) of South Asia and is a disease of major concern in other similar wheat growing regions worldwide. Differential lignin content in resistant and susceptible genotypes and its association with free radicals such as hydrogen peroxide ($H_2O_2$), superoxide ($O_2{^-}$) and hydroxyl radical ($OH^-$) were studied after inoculation under field conditions for two consecutive years. $H_2O_2$ significantly influenced lignin content in flag leaves, whereas there was a negative correlation among lignin and $H_2O_2$ to the Area Under Disease Progress Curve (AUDPC). The production of $H_2O_2$ was higher in the resistant genotypes than susceptible ones. The $O_2{^-}$ and $OH^-$ positively correlated with AUDPC but negatively with lignin content. This study illustrates that $H_2O_2$ has a vital role in prompting lignification and thereby resistance to spot blotch in wheat. We used cluster analysis to separate the resistant and susceptible genotypes by phenotypic and biochemical traits. $H_2O_2$ associated lignin production significantly reduced the number of appressoria and penetration pegs. We visualized the effect of lignin in disease resistance using differential histochemical staining of tissue from resistant and susceptible genotypes, which shows the variable accumulation of hydrogen peroxide and lignin around penetration sites.
Keywords
lignin; reactive oxygen species; resistance; spot blotch;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Halliwell, B., Gutteridge, J. M. and Aruoma, O. I. 1987. The deoxyribose method: a simple "test-tube" assay for determination of rate constants for reactions of hydroxyl radicals. Anal. Biochem. 165:215-219.   DOI
2 Jacobo-Velazquez, D. A., Gonzalez-Aguero, M. and Cisneros-Zevallos, L. 2015. Cross-talk between signaling pathways:the link between plant secondary metabolite production and wounding stress response. Sci. Rep. 5:8608.   DOI
3 Joshi, A. K. and Chand, R. 2002. Variation and inheritance of leaf angle, and its association with spot blotch Bipolaris sorokiniana severity in wheat Triticum aestivum. Euphytica 124:283-291.   DOI
4 Joshi, A. K., Chand, R. and Arun, B. 2002. Relationship of plant height and days to maturity with resistance to spot blotch in wheat. Euphytica 123:221-228.   DOI
5 Joshi, A. K., Kumar, S., Chand, R. and Ortiz-Ferrara, G. 2004. Inheritance of resistance to spot blotch caused by Bipolaris sorokiniana in spring wheat. Plant Breed. 123:213-219.   DOI
6 Kumar, J., Schafer, P., Huckelhoven, R., Langen, G., Baltruschat, H., Stein, E., Nagarajan, S. and Kogel, K.-H. 2002. Bipolaris sorokiniana, a cereal pathogen of global concern: cytological and molecular approaches towards better control. Mol. Plant Pathol. 3:185-195.   DOI
7 Levene, H. 1960. Robust tests for equality of variances. In: Contributions to probability and statistics, ed. by I. Olkin, pp. 278-292. Stanford University Press, Palo Alto, CA, USA.
8 Lightfoot, D. J., McGrann, G. R. and Able, A. J. 2017. The role of a cytosolic superoxide dismutase in barley-pathogen interactions. Mol. Plant Pathol. 18:323-335.   DOI
9 Marschall, R. and Tudzynski, P. 2016. Reactive oxygen species in development and infection processes. Semin. Cell Dev. Biol. 57:138-146.   DOI
10 Mehta, Y. R. 1998. Constraints on the integrated management of spot blotch of wheat. In: Helminthosporium blights of wheat:Spot blotch and tan spot, eds. by E. Duveiller, H. J. Dubin, J. Reeves and A. McNab, pp. 18-27. International Maize and Wheat Improvement Center, Mexico City, Mexico.
11 Mellersh, D. G., Foulds, I. V., Higgins, V. J. and Heath, M. C. 2002. $H_2O_2$ plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J. 29:257-268.   DOI
12 Miedes, E., Vanholme, R., Boerjan, W. and Molina, A. 2014. The role of the secondary cell wall in plant resistance to pathogens. Front. Plant Sci. 5:358.
13 Milus, E. A. and Line, R. F. 1980. Characterization of resistance to leaf rust in Pacific Northwest wheats. Phytopathology 70:167-172.   DOI
14 Misra, H. P. and Fridovich, I. 1972. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 247:3170-3175.   DOI
15 Patterson, B. D., MacRae, E. A. and Ferguson, I. B. 1984. Estimation of hydrogen peroxide in plant extracts using titanium IV. Anal. Biochem. 139:487-492.   DOI
16 Aldaeus, F. 2011. Protocol for round robin test of lignin content in lignin samples COST FP0901. URL http://web.abo.fi/fak/tkf/spk/costfp0901/Round_robin/COST_FP0901-Protocol_for_round_robin_test_of_lignin_content-version_3.pdf [6 July 2019].
17 Apel, K. and Hirt, H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373-399.   DOI
18 Bashyal, B. M., Chand, R., Prasad, L. C. and Joshi, A. K. 2011. Partial resistance components for the management of spot blotch pathogen Bipolaris sorokiniana of barley (Hordeum vulgare L.) Acta Phytopathol. Entomol. Hung. 46:49-57.   DOI
19 Nicholson, R. L. and Hammerschmidt, R. 1992. Phenolic compounds and their role in disease resistance. Annu. Rev. Phytopathol. 30:369-389.   DOI
20 Parlevliet, J. E. 1979. Components of resistance that reduce the rate of epidemic development. Annu. Rev. Phytopathol. 17:203-222.   DOI
21 Purwar, S., Gupta, S. M. and Kumar, A. 2012. Enzymes of phenylpropanoid metabolism involved in strengthening the structural barrier for providing genotype and stage-dependent resistance to Karnal bunt in wheat. Am. J. Plant Sci. 3:261-267.   DOI
22 Boerjan, W., Ralph, J. and Baucher, M. 2003. Lignin biosynthesis. Annu. Rev. Plant Biol. 54:519-546.   DOI
23 Beardmore, J., Ride, J. P. and Granger, J. W. 1983. Cellular lignification as a factor in the hypersensitive resistance of wheat to stem rust. Physiol. Plant Pathol. 22:209-220.   DOI
24 Bhuiyan, N. H., Selvaraj, G., Wei, Y. and King, J. 2009. Role of lignification in plant defense. Plant Signal Behav. 4:158-159.   DOI
25 Bingham, I. J., Walters, D. R., Foulkes, M. J. and Paveley, N. D. 2009. Crop traits and the tolerance of wheat and barley to foliar disease. Ann. Appl. Biol. 154:159-173.   DOI
26 Bird, P. M. and Ride, J. P. 1981. The resistance of wheat to Septoria nodorum: fungal development in relation to host lignification. Physiol. Plant Pathol. 19:289-299.   DOI
27 Bishop, D. L., Chatterton, N. J., Harrison, P. A. and Hatfield, R. D. 2002. Changes in carbohydrate coordinated partitioning and cell wall remodeling with stress-induced pathogenesis in wheat sheaths. Physiol. Mol. Plant Pathol. 61:53-63.   DOI
28 Boudet, A. M. 2000. Lignins and lignification: selected issues. Plant Physiol. Biochem. 38:81-96.   DOI
29 Cano-Delgado, A., Penfield, S., Smith, C., Catley, M. and Bevan, M. 2003. Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. Plant J. 34:351-362.   DOI
30 Chand, R., Yadav, O. P., Bashyal, B. M., Prasad, L. C. and Joshi, A. K. 2013. Technique for the maintenance of heterokaryotic isolates of B. sorokiniana. Indian Phytopathol. 66:61-65.
31 Das, M. K., Rajaram, S., Kronstad, W. E., Mundt, C. C. and Singh, R. P. 1993. Associations and genetics of three components of slow rusting in leaf rust of wheat. Euphytica 68:99-109.   DOI
32 Eisa, M., Chand, R. and Joshi, A. K. 2013. Biochemical and histochemical traits: a promising way to screen resistance against spot blotch Bipolaris sorokiniana of wheat. Eur. J. Plant Pathol. 137:805-820.   DOI
33 Denness, L., McKenna, J. F., Segonzac, C., Wormit, A., Madhou, P., Bennett, M., Mansfield, J., Zipfel, C. and Hamann, T. 2011. Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species-and jasmonic aciddependent process in Arabidopsis. Plant Physiol. 156:1364-1374.   DOI
34 Dixon, R. A., Chen, F., Guo, D. and Parvathi, K. 2001. The biosynthesis of monolignols: A "metabolic grid", or independent pathways to guaiacyl and syringyl units? Phytochemistry 57:1069-1084.   DOI
35 Dubin, H. J. and van Ginkel, M. 1991. The status of wheat diseases and disease research in warmer areas. In: Wheat for the nontraditional warm areas: A proceedings of the International Conference, ed. by D. A. Saunders, pp. 125-145. International Maize and Wheat Improvement Center, Mexico City, Mexico.
36 Elad, Y. and Evensen, K. 1995. Physiological aspects of resistance to Botrytis cinerea. Phytopathology 85:637-643.
37 Gupta, P. K., Chand, R., Vasistha, N. K., Pandey, S. P., Kumar, U., Mishra, V. K. and Joshi, A. K. 2018. Spot blotch disease of wheat: the current status of research on genetics and breeding. Plant Pathol. 67:508-531.   DOI
38 Gurung, S., Mahto, B. N., Gyawali, S. and Adhikari, T. B. 2013. Phenotypic and molecular diversity of Cochliobolus sativus populations from wheat. Plant Dis. 97:62-73.   DOI
39 Hakmaoui, A., Perez-Bueno, M. L., Garcia-Fontana, B., Camejo, D., Jimenez, A., Sevilla, F. and Baron, M. 2012. Analysis of the antioxidant response of Nicotiana benthamiana to infection with two strains of Pepper mild mottle virus. J. Exp. Bot. 63:5487-5496.   DOI
40 Shapiro, S. S. and Wilk, M. B. 1965. An analysis of variance test for normality (complete samples). Biometrika 52:591-611.   DOI
41 Sharma, S., Sahu, R., Navathe, S., Mishra, V. K., Chand, R., Singh, P. K., Joshi, A. K. and Pandey, S. P. 2018. Natural variation in elicitation of defense-signaling associates to field resistance against the spot blotch disease in bread wheat (Triticum aestivum L.). Front. Plant Sci. 9:636.   DOI
42 Shetty, N. P., Mehrabi, R., Lutken, H., Haldrup, A., Kema, G. H., Collinge, D. B. and Jorgensen, H. J. 2007. Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat. New Phytol. 174:637-647.   DOI
43 Sillero, J. C. and Rubiales, D. 2002. Histological characterization of resistance to Uromyces viciae-fabae in faba bean. Phytopathology 92:294-299.   DOI
44 Singh, P. K., Zhang, Y., He, X., Singh, R. P., Chand, R., Mishra, V. K., Malaker, P. K., Reza, M. A., Rahman, M. M., Islam, R., Chowdhury, A. K., Bhattacharya, P. M., Kalappanavar, I. K., Crossa, J. and Joshi, A. K. 2015. Development and characterization of the 4th CSISA-spot blotch nursery of bread wheat. Eur. J. Plant Pathol. 143:595-605.   DOI
45 Wu, G., Shortt, B. J., Lawrence, E. B., Leon, J., Fitzsimmons, K. C., Levine, E. B., Raskin, I. and Shah, D. M. 1997. Activation of host defense mechanisms by elevated production of $H_2O_2$ in transgenic plants. Plant Physiol. 115:427-435.   DOI
46 Southerton, S. G. and Deverall, B. J. 1990. Histochemical and chemical evidence for lignin accumulation during the expression of resistance to leaf rust fungi in wheat. Physiol. Mol. Plant Pathol. 36:483-494.   DOI
47 Thordal-Christensen, H., Zhang, Z., Wei, Y. and Collinge, D. B. 1997. Subcellular localization of $H_2O_2$ in plants. $H_2O_2$ accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11:1187-1194.   DOI
48 Tomerlin, J. R., Eversmeyer, M. G., Kramer, C. L. and Browder, L. E. 1983. Temperature and host effects on latent and infectious periods and urediniospore production of Puccinia recondita f. sp. tritici. Phytopathology 73:414-419.   DOI
49 Tronchet, M., Balague, C., Kroj, T., Jouanin, L. and Roby, D. 2010. Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis. Mol. Plant Pathol. 11:83-92.   DOI
50 Willocquet, L., Savary, S. and Yuen, J. 2017. Multiscale phenotyping and decision strategies in breeding for resistance. Trends Plant Sci. 22:420-432.   DOI
51 Yusuf, C. S., Chand, R., Mishra, V. K. and Joshi, A. K. 2016. The association between leaf malondialdehyde and lignin content and resistance to spot blotch in wheat. J. Phytopathol. 164:896-903.   DOI
52 Zadoks, J. C., Chang, T. T. and Konzak, C. F. 1974. A decimal code for the growth stages of cereals. Weed Res. 14:415-421.   DOI
53 Shaner, G. and Finney, R. E. 1977. The effect of nitrogen fertilization on the expression of slow-mildewing in Knox wheat. Phytopathology 67:1051-1056.   DOI
54 Ros Barcelo, A. 2005. Xylem parenchyma cells deliver the $H_2O_2$ necessary for lignification in differentiating xylem vessels. Planta 220:747-756.   DOI
55 Schafer, P., Huckelhoven, R. and Kogel, K. H. 2004. The white barley mutant albostrians shows a super-susceptible but symptomless interaction phenotype with the hemibiotrophic fungus Bipolaris sorokiniana. Mol. Plant-Microbe Interact. 17:366-373.   DOI