A novel pathogenicity determinant hijacks maize catalase 1 to enhance viral multiplication and infection.

Zea mays catalase maize chlorotic mottle virus (MCMV) pathogenesis-related (PR) protein salicylic acid (SA)-mediated defence systemic necrosis

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
05 2021
Historique:
received: 17 11 2020
accepted: 07 01 2021
pubmed: 19 1 2021
medline: 15 5 2021
entrez: 18 1 2021
Statut: ppublish

Résumé

Pathogens have evolved various strategies to overcome host immunity for successful infection. Maize chlorotic mottle virus (MCMV) can cause lethal necrosis in maize (Zea mays) when it coinfects with a virus in the Potyviridae family. However, the MCMV pathogenicity determinant remains largely unknown. Here we show that the P31 protein of MCMV is important for viral accumulation and essential for symptom development. Ectopic expression of P31 using foxtail mosaic virus or potato virus X induced necrosis in systemically infected maize or Nicotiana benthamiana leaves. Maize catalases (CATs) were shown to interact with P31 in yeast and in planta. P31 accumulation was elevated through its interaction with ZmCAT1. P31 attenuated the expression of salicylic acid (SA)-responsive pathogenesis-related (PR) genes by inhibiting catalase activity during MCMV infection. In addition, silencing of ZmCATs using a brome mosaic virus-based gene silencing vector facilitated MCMV RNA and coat protein accumulation. This study reveals an important role for MCMV P31 in counteracting host defence and inducing systemic chlorosis and necrosis. Our results have implications for understanding the mechanisms in defence and counter-defence during infection of plants by various pathogens.

Identifiants

pubmed: 33458828
doi: 10.1111/nph.17206
doi:

Substances chimiques

Catalase EC 1.11.1.6
Salicylic Acid O414PZ4LPZ

Banques de données

RefSeq
['NM_001254879.2', 'NM_001111840.2', 'NM_001363892.1', 'NM_001367877.1', 'EU970195.1']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1126-1141

Informations de copyright

© 2021 The Authors New Phytologist © 2021 New Phytologist Foundation.

Références

Adams IP, Miano DW, Kinyua ZM, Wangai A, Kimani E, Phiri N, Reeder R, Harju V, Glover R, Hany U. 2013. Use of next-generation sequencing for the identification and characterization of maize chlorotic mottle virus and sugarcane mosaic virus causing maize lethal necrosis in Kenya. Plant Pathology 62: 741-749.
Aebi H. 1984. Catalase in vitro. Methods in Enzymology 105: 121-126.
Alazem M, Lin NS. 2015. Roles of plant hormones in the regulation of host-virus interactions. Molecular Plant Pathology 16: 529-540.
Baebler S, Stare K, Kovac M, Blejec A, Prezelj N, Stare T, Kogovsek P, Pompe-Novak M, Rosahl S, Ravnikar M et al. 2011. Dynamics of responses in compatible potato - potato virus Y interaction are modulated by salicylic acid. PLoS ONE 6: e29009.
Baebler S, Witek K, Petek M, Stare K, Tusek-Znidaric M, Pompe-Novak M, Renaut J, Szajko K, Strzelczyk-Zyta D, Marczewski W et al. 2014. Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against potato virus Y infection in potato. Journal of Experimental Botany 65: 1095-1109.
Bouton C, King RC, Chen H, Azhakanandam K, Bieri S, Hammond-Kosack KE, Kanyuka K. 2018. Foxtail mosaic virus: a viral vector for protein expression in cereals. Plant Physiology 177: 1352-1367.
Braidwood L, Quito-Avila DF, Cabanas D, Bressan A, Wangai A, Baulcombe DC. 2018. Maize chlorotic mottle virus exhibits low divergence between differentiated regional sub-populations. Scientific Reports 8: 1173.
Cao N, Zhan B, Zhou X. 2019. Nitric oxide as a downstream signalling molecule in brassinosteroid-mediated virus susceptibility to maize chlorotic mottle virus in maize. Viruses 11: 386.
Cao Y, Shi Y, Li Y, Cheng Y, Zhou T, Fan Z. 2012. Possible involvement of maize Rop1 in the defence responses of plants to viral infection. Molecular Plant Pathology 13: 732-743.
Carino EJ, Scheets K, Miller WA. 2020. The RNA of maize chlorotic mottle virus, an obligatory component of maize lethal necrosis disease, is translated via a variant panicum mosaic virus-like cap-independent translation element. Journal of Virology 94: e01005-20.
Chen H, Zou Y, Shang Y, Lin H, Wang Y, Cai R, Tang X, Zhou JM. 2008. Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiology 146: 368-376.
Chen L, Yan Z, Xia Z, Cheng Y, Jiao Z, Sun B, Zhou T, Fan Z. 2017. A violaxanthin deepoxidase interacts with a viral suppressor of RNA silencing to inhibit virus amplification. Plant Physiology 175: 1774-1794.
Chen ZX, Silva H, Klessig DF. 1993. Active oxygen species in the induction of plant systemic acquired-resistance by salicylic acid. Science 262: 1883-1886.
Dinesh-Kumar SP, Tham WH, Baker BJ. 2000. Structure-function analysis of the tobacco mosaic virus resistance gene N. Proceedings of the National Academy of Sciences, USA 97: 14789-14794.
van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J et al. 2011. Morphological classification of plant cell deaths. Cell Death & Differentiation 18: 1241-1246.
Fentahun M, Feyissa T, Abraham A, Kwak HR. 2017. Detection and characterization of maize chlorotic mottle virus and sugarcane mosaic virus associated with maize lethal necrosis disease in Ethiopia: an emerging threat to maize production in the region. European Journal of Plant Pathology 149: 1011-1017.
Garcia JA, Pallas V. 2015. Viral factors involved in plant pathogenesis. Current Opinion in Virology 11: 21-30.
Goldberg KB, Brakke MK. 1987. Concentration of maize chlorotic mottle virus increased in mixed infections with maize dwarf mosaic virus, strain B. Phytopathology 77: 162-167.
Goodin MM, Dietzgen RG, Schichnes D, Ruzin S, Jackson AO. 2002. pGD vectors: versatile tools for the expression of green and red fluorescent protein fusions in agroinfiltrated plant leaves. The Plant Journal 31: 375-383.
Hafez YM, Bacso R, Kiraly Z, Kunstler A, Kiraly L. 2012. Up-regulation of antioxidants in tobacco by low concentrations of H2O2 suppresses necrotic disease symptoms. Phytopathology 102: 848-856.
Inaba J, Kim BM, Shimura H, Masuta C. 2011. Virus-induced necrosis is a consequence of direct protein-protein interaction between a viral RNA-silencing suppressor and a host catalase. Plant Physiology 156: 2026-2036.
Jameson PE, Clarke SF. 2002. Hormone-virus interactions in plants. Critical Reviews in Plant Sciences 21: 205-228.
Ji LH, Ding SW. 2001. The suppressor of transgene RNA silencing encoded by cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Molecular Plant-Microbe Interactions 14: 715-724.
Király Z, Barna B, Érsek T. 1972. Hypersensitivity as a consequence, not the cause, of plant resistance to infection. Nature 239: 456-458.
Komatsu K, Hashimoto M, Ozeki J, Yamaji Y, Maejima K, Senshu H, Himeno M, Okano Y, Kagiwada S, Namba S. 2010. Viral-induced systemic necrosis in plants involves both programmed cell death and the inhibition of viral multiplication, which are regulated by independent pathways. Molecular Plant-Microbe Interactions 23: 283-293.
Lee WS, Fu SF, Verchot-Lubicz J, Carr JP. 2011. Genetic modification of alternative respiration in Nicotiana benthamiana affects basal and salicylic acid-induced resistance to potato virus X. BMC Plant Biology 11: 41.
Liu Y, Schiff M, Czymmek K, Talloczy Z, Levine B, Dinesh-Kumar SP. 2005. Autophagy regulates programmed cell death during the plant innate immune response. Cell 121: 567-577.
Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402-408.
Love AJ, Geri C, Laird J, Carr C, Yun BW, Loake GJ, Tada Y, Sadanandom A, Milner JJ. 2012. Cauliflower mosaic virus protein P6 inhibits signalling responses to salicylic acid and regulates innate immunity. PLoS ONE 7: e47535.
Lu YW, Yin MY, Wang XD, Chen BH, Yang X, Peng JJ, Zheng HY, Zhao JP, Lin L, Yu CL et al. 2016. The unfolded protein response and programmed cell death are induced by expression of garlic virus X p11 in Nicotiana benthamiana. Journal of General Virology 97: 1462-1468.
Lukan T, Baebler S, Pompe-Novak M, Gucek K, Zagorscak M, Coll A, Gruden K. 2018. Cell death is not sufficient for the restriction of potato virus Y spread in hypersensitive response-conferred resistance in potato. Frontiers in Plant Science 9: 168.
Magbanua ZV, De Moraes CM, Brooks TD, Williams WP, Luthe DS. 2007. Is catalase activity one of the factors associated with maize resistance to Aspergillus flavus? Molecular Plant-Microbe Interactions 20: 697-706.
Malamy J, Carr JP, Klessig DF, Raskin I. 1990. Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1002-1004.
Mandadi KK, Scholthof KB. 2013. Plant immune responses against viruses: how does a virus cause disease? The Plant Cell 25: 1489-1505.
Mathioudakis MM, Veiga RS, Canto T, Medina V, Mossialos D, Makris AM, Livieratos I. 2013. Pepino mosaic virus triple gene block protein 1 (TGBp1) interacts with and increases tomato catalase 1 activity to enhance virus accumulation. Molecular Plant Pathology 14: 589-601.
Murota K, Shimura H, Takeshita M, Masuta C. 2017. Interaction between cucumber mosaic virus 2b protein and plant catalase induces a specific necrosis in association with proteasome activity. Plant Cell Reports 36: 37-47.
Murphy AM, Zhou T, Carr JP. 2020. An update on salicylic acid biosynthesis, its induction and potential exploitation by plant viruses. Current Opinion in Virology 42: 8-17.
Ndamukong I, Al Abdallat A, Thurow C, Fode B, Zander M, Weigel R, Gatz C. 2007. SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. The Plant Journal 50: 128-139.
Niehl A, Wyrsch I, Boller T, Heinlein M. 2016. Double-stranded RNAs induce a pattern-triggered immune signalling pathway in plants. New Phytologist 211: 1008-10191008-1019.
Pan XQ, Welti R, Wang XM. 2010. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nature Protocols 5: 986-992.
Qi G, Chen J, Chang M, Chen H, Hall K, Korin J, Liu F, Wang D, Fu ZQ. 2018. Pandemonium breaks out: disruption of salicylic acid-mediated defense by plant pathogens. Molecular Plant 11: 1427-1439.
Redinbaugh MG, Sabre M, Scandalios JG. 1990. The distribution of catalase activity, isozyme protein, and transcript in the tissues of the developing maize seedling. Plant Physiology 92: 375-380.
Redinbaugh MG, Stewart LR. 2018. Maize lethal necrosis: an emerging, synergistic viral disease. Annual Review of Virology 5: 301-322.
Roshan P, Kulshreshtha A, Kumar S, Purohit R, Hallan V. 2018. AV2 protein of tomato leaf curl Palampur virus promotes systemic necrosis in Nicotiana benthamiana and interacts with host catalase 2. Scientific Reports 8: 1273.
Roupakias DG, Mcmillin DE, Scandalios JG. 1980. Chromosomal location of the catalase structural genes in Zea mays using B-A translocations. Theoretical and Applied Genetics 58: 211-218.
Scandalios JG, Tsaftaris AS, Chandlee JM, Skadsen RW. 1984. Expression of the developmentally regulated catalase (cat) genes in maize. Developmental Genetics 4: 281-293.
Scheets K. 1998. Maize chlorotic mottle machlomovirus and wheat streak mosaic rymovirus concentrations increase in the synergistic disease corn lethal necrosis. Virology 242: 28-38.
Scheets K. 2016. Analysis of gene functions in maize chlorotic mottle virus. Virus Research 222: 71-79.
Scheets K, Khosravifar R, Nutter RC. 1993. Transcripts of a maize chlorotic mottle virus cDNA clone replicate in maize protoplasts and infect maize plants. Virology 193: 1006-1009.
Schmidt A, Machtel R, Ammon A, Engelsdorf T, Schmitz J, Maurino VG, Voll LM. 2020. Reactive oxygen species dosage in Arabidopsis chloroplasts can improve resistance towards Colletotrichum higginsianum by the induction of WRKY33. New Phytologist 226: 189-204.
Smadar PG, Naomi MB, Gil C, Alex L. 2010. Cytoplasmic H2O2 prevents translocation of NPR1 to the nucleus and inhibits the induction of PR genes in Arabidopsis. Plant Signalling & Behavior 5: 1401-1406.
Spoel SH, Dong X. 2008. Making sense of hormone crosstalk during plant immune responses. Cell Host & Microbe 3: 348-351.
Stewart LR, Willie K, Wijeratne S, Redinbaugh P, Massawe DP, Niblett CL, Kiggundu A, Asiimwe T. 2017. Johnsongrass mosaic virus contributes to maize lethal necrosis in east Africa. Plant Disease 101: 1455-1462.
Thordal-Christensen H, Zhang ZG, Wei YD, Collinge DB. 1997. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal 11: 1187-1194.
Vlot AC, Dempsey DA, Klessig DF. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology 47: 177-206.
Wadsworth GJ, Scandalios JG. 1989. Differential expression of the maize catalase genes during kernel development: the role of steady-state mRNA levels. Developmental Genetics 10: 304-310.
Wang Q, Zhang C, Wang C, Qian Y, Li Z, Hong J, Zhou X. 2017. Further characterization of maize chlorotic mottle virus and its synergistic interaction with sugarcane mosaic virus in maize. Scientific Reports 7: 39960.
Wu CH, Abd-El-Haliem A, Bozkurt TO, Belhaj K, Terauchi R, Vossen JH, Kamoun S. 2017. NLR network mediates immunity to diverse plant pathogens. Proceedings of the National Academy of Sciences, USA 114: 8113-8118.
Xia Z, Zhao Z, Chen L, Li M, Zhou T, Deng C, Zhou Q, Fan Z. 2016. Synergistic infection of two viruses MCMV and SCMV increases the accumulations of both MCMV and MCMV-derived siRNAs in maize. Scientific Reports 6: 20520.
Xu P, Roossinck MJ. 2000. Cucumber mosaic virus D satellite RNA-induced programmed cell death in tomato. The Plant Cell 12: 1079-1092.
Yang T, Qiu L, Huang W, Xu Q, Zou J, Peng Q, Lin H, Xi D. 2020. Chilli veinal mottle virus HCPro interacts with catalase to facilitate virus infection in Nicotiana tabacum. Journal of Experimental Botany 71: 5656-5668.
Yao N, Imai S, Tada Y, Nakayashiki H, Tosa Y, Park P, Mayama S. 2002. Apoptotic cell death is a common response to pathogen attack in oats. Molecular Plant-Microbe Interactions 15: 1000-1007.
Yuan HM, Liu WC, Lu YT. 2017. CATALASE2 coordinates SA-mediated repression of both auxin accumulation and JA biosynthesis in plant defenses. Cell Host & Microbe 21: 143-155.
Zavaliev R, Mohan R, Chen TY, Dong XN. 2020. Formation of NPR1 condensates promotes cell survival during the plant immune response. Cell 182: 1093-1108.
Zhang M, Li Q, Liu T, Liu L, Shen D, Zhu Y, Liu P, Zhou JM, Dou D. 2015. Two cytoplasmic effectors of Phytophthora sojae regulate plant cell death via interactions with plant catalases. Plant Physiology 167: 164-175.
Zhao YN, Luo LL, Xu JS, Xin PY, Guo HY, Wu J, Bai L, Wang GD, Chu JF, Zuo JR et al. 2018. Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana. Cell Research 28: 448-461.
Zhou YB, Liu C, Tang DY, Yan L, Wang D, Yang YZ, Gui JS, Zhao XY, Li LG, Tang XD et al. 2018. The receptor-like cytoplasmic kinase STRK1 phosphorylates and activates CatC, thereby regulating H2O2 homeostasis and improving salt tolerance in rice. The Plant Cell 30: 1100-1118.
Zhu M, Chen Y, Ding XS, Webb SL, Zhou T, Nelson RS, Fan Z. 2014. Maize Elongin C interacts with the viral genome-linked protein, VPg, of sugarcane mosaic virus and facilitates virus infection. New Phytologist 203: 1291-1304.
Ziemann S, van der Linde K, Lahrmann U, Acar B, Kaschani F, Colby T, Kaiser M, Ding YZ, Schmelz E, Huffaker A et al. 2018. An apoplastic peptide activates salicylic acid signalling in maize. Nature Plants 4: 172-180.

Auteurs

Zhiyuan Jiao (Z)

State Kay Laboratory of Agrobiotechnology and Key Laboratory of Pest Monitoring and Green Management-MOA, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China.

Yiying Tian (Y)

State Kay Laboratory of Agrobiotechnology and Key Laboratory of Pest Monitoring and Green Management-MOA, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China.

Yanyong Cao (Y)

Cereal Crops Institute, Henan Academy of Agricultural Sciences, Zhengzhou, 450002, China.

Juan Wang (J)

State Kay Laboratory of Agrobiotechnology and Key Laboratory of Pest Monitoring and Green Management-MOA, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China.

Binhui Zhan (B)

State Kay Laboratory of Agrobiotechnology and Key Laboratory of Pest Monitoring and Green Management-MOA, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China.

Zhenxing Zhao (Z)

State Kay Laboratory of Agrobiotechnology and Key Laboratory of Pest Monitoring and Green Management-MOA, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China.

Biao Sun (B)

State Kay Laboratory of Agrobiotechnology and Key Laboratory of Pest Monitoring and Green Management-MOA, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China.

Chang Guo (C)

State Kay Laboratory of Agrobiotechnology and Key Laboratory of Pest Monitoring and Green Management-MOA, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China.

Wendi Ma (W)

State Kay Laboratory of Agrobiotechnology and Key Laboratory of Pest Monitoring and Green Management-MOA, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China.

Zhenfeng Liao (Z)

State Key Laboratory for Sustainable Control of Pest and Disease, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, China.

Hengmu Zhang (H)

State Key Laboratory for Sustainable Control of Pest and Disease, Institute of Virology and Biotechnology, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, China.

Tao Zhou (T)

State Kay Laboratory of Agrobiotechnology and Key Laboratory of Pest Monitoring and Green Management-MOA, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China.

Yiji Xia (Y)

Department of Biology, Hong Kong Baptist University, Hong Kong SAR, China.
State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong SAR, China.

Zaifeng Fan (Z)

State Kay Laboratory of Agrobiotechnology and Key Laboratory of Pest Monitoring and Green Management-MOA, Department of Plant Pathology, China Agricultural University, Beijing, 100193, China.

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