|
|
|
|
|
| Recent advances in plant immunity with cell death: A review |
| YIN Jun-jie, XIONG Jun, XU Li-ting, CHEN Xue-wei, LI Wei-tao |
| State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Rice Research Institute, Sichuan Agricultural University at Wenjiang, Chengdu 611130, P.R.China
|
|
|
|
|
摘要
细胞死亡是多细胞生物生命中一种重要的生理现象。当呼吸和新陈代谢等正常功能停止时，将会发生细胞死亡。细胞死亡可分为程序性细胞死亡和非程序性细胞死亡。正常组织中发生的程序性细胞死亡，通常是维持组织机能和形态所必须的。非程序性细胞死亡则通常由非生物或生物胁迫引起。近年来，大量研究报道植物在抵御病原菌时出现了细胞死亡现象。通过分析调控植物免疫反应和细胞死亡的蛋白（PICD），发现PICD主要参与丝裂原活化蛋白激酶（MAPK）级联、活性氧（ROS）、植物激素、泛素-蛋白酶体系统、Ca2+信号、物质转运等六种主要的反应过程，且这些反应过程存在内在的联系。同时，PICD主要分为八类，如：含有核苷酸结合结构域和富含亮氨酸重复序列的蛋白（NLR）蛋白、受体或类受体激酶、E3泛素连接酶和其相关蛋白、ATP和GTP相关蛋白、转录因子、14-3-3蛋白和其相关蛋白、类eEF1A蛋白和丝氨酸蛋白酶抑制子，部分PICD类型具有单、双子叶植物特异性。植物细胞死亡不仅与病原相关分子模式激发的免疫反应（PTI）、效应因子激发的免疫反应（ETI）紧密相关，也与系统获得性抗性（SAR）存在重要关联。PICD在细胞外基质、细胞膜、细胞质、细胞核、线粒体、叶绿体、内质网膜、多囊泡体等众多细胞结构中均有分布，表明细胞在应对病原菌侵染和调控自身死亡时存在精妙地协同调控作用。此外，植物在抵御病原菌时的细胞死亡，通常对其自身的生长发育不利。通过筛选优异的等位变异和基因编辑等技术手段，期望达到植物免疫和生长发育间的平衡，以此增强PICD在植物应用领域中的潜力。
Abstract Cell death is an important physiological phenomenon in life. It can be programmed or unprogrammed. Unprogrammed cell death is usually induced by abiotic or biotic stress. Recent studies have shown that many proteins regulate both cell death and immunity in plants. Here, we provide a review on the advances in plant immunity with cell death, especially the molecular regulation and underlying mechanisms of those proteins involved in both cell death and plant immunity. In addition, we discuss potential approaches toward improving plant immunity without compromising plant growth.
|
|
Received: 14 January 2021
Accepted: 06 May 2021
|
| Fund: This work was supported by the National Natural Science Foundation of China (NSFC, 31972254), the Fok Ying Tung Education Foundation (171021), the Tianfu Ten-thousand Talents Program (Tianfu Science and Technology Elite Project), China, the Outstanding Young Scientific and Technological Talents Project in Sichuan Province, China (2019JDJQ0045), and Outstanding Youth Science Foundation of Sichuan Agricultural University, China (2021SZYQ002) to Li Weitao; the Key R&D Projects of Science & Technology Department of Sichuan Province (2018JZ0072); NSFC (31825022) to Chen Xuewei; and the NSFC (32072041) to Yin Junjie. |
| About author: Correspondence LI Wei-tao, Tel: +86-28-86291189, E-mail: weitao-li@sicau.edu.cn
* These authors contributed equally to this study. |
Cite this article:
YIN Jun-jie, XIONG Jun, XU Li-ting, CHEN Xue-wei, LI Wei-tao.
2022.
Recent advances in plant immunity with cell death: A review. Journal of Integrative Agriculture, 21(3): 610-620.
|
Acevedo-Garcia J, Spencer D, Thieron H, Reinstadler A, Hammond-Kosack K, Phillips A L, Panstruga R. 2017. mlo-based powdery mildew resistance in hexaploid bread wheat generated by a non-transgenic TILLING approach. Plant Biotechnology Journal, 15, 367–378.
Barlow P W. 1982. Cell Death - An Intergral Part of Plant Development. In Growth Regulators in Plant Senescence. British Plant Growth Regulator Group, Wantage, UK. pp. 27–45.
Baudin M, Hassan J A, Schreiber K J, Lewis J D. 2017. Analysis of the ZAR1 immune complex reveals determinants for immunity and molecular interactions. Plant Physiology, 174, 2038–2053.
Bhattacharjee L, Singh D, Gautam J K, Nandi A K. 2017. Arabidopsis thaliana serpins AtSRP4 and AtSRP5 negatively regulate stress-induced cell death and effector-triggered immunity induced by bacterial effector AvrRpt2. Physiologia Plantarum, 159, 329–339.
Bolus S, Akhunov E, Coaker G, Dubcovsky J. 2020. Dissection of cell death induction by wheat stem rust resistance protein Sr35 and its matching effector AvrSr35. Molecular Plant (Microbe Interaction), 33, 308–319.
Brown D A, Yang N, Ray S D. 2014. Encyclopedia of Toxicology. 3rd ed. Elsevier Inc., Netherlands. pp. 287–294.
Cai J, Chen T, Wang Y, Qin G, Tian S. 2020. SlREM1 triggers cell death by activating an oxidative burst and other regulators. Plant Physiology, 183, 717–732.
Cao J, Zhang M, Zhu M, He L, Xiao J, Li X, Yuan M. 2019. Autophagy-like cell death regulates hydrogen peroxide and calcium ion distribution in Xa3/Xa26-mediated resistance to Xanthomonas oryzae pv. oryzae. International Journal of Molecular Sciences, 21, 1.
Cesari S, Kanzaki H, Fujiwara T, Bernoux M, Chalvon V, Kawano Y, Shimamoto K, Dodds P, Terauchi R, Kroj T. 2014. The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO Journal, 33, 1941–1959.
Cesari S, Moore J, Chen C, Webb D, Periyannan S, Mago R, Bernoux M, Lagudah E S, Dodds P N. 2016. Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC-NLR proteins. Proceedings of the National Academy of Sciences of the United States of America, 113, 10204–10209.
Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones J D, Felix G, Boller T.2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature, 448, 497–500.
Choi H W, Kim Y J, Hwang B K. 2011. The hypersensitive induced reaction and leucine-rich repeat proteins regulate plant cell death associated with disease and plant immunity. Molecular Plant (Microbe Interaction), 24, 68–78.
Dang T T, Shimatani Z, Kawano Y, Terada R, Shimamoto K. 2013. Gene editing a constitutively active OsRac1 by homologous recombination-based gene targeting induces immune responses in rice. Plant Cell Physiology, 54, 2058–2070.
D’Arcy M S. 2019. Cell death: A review of the major forms of apoptosis, necrosis and autophagy. Cell Biology International, 43, 582–592.
Eichmann R, Schafer R. 2012. The endoplasmic reticulum in plant immunity and cell death. Frontiers in Plant Science, 3, 200.
Fan J, Bai P, Ning Y, Wang J, Shi X, Xiong Y, Zhang K, He F, Zhang C, Wang R, Meng X, Zhou J, Wang M, Shirsekar G, Park C H, Bellizzi M, Liu W, Jeon J S, Xia Y, Shan L, et al. 2018. The monocot-specific receptor-like kinase SDS2 controls cell death and immunity in rice. Cell Host and Microbe, 23, 498–510.
Fukunaga S, Sogame M, Hata M, Singkaravanit-Ogawa S, Pislewska-Bednarek M, Onozawa-Komori M, Nishiuchi T, Hiruma K, Saitoh H, Terauchi R, Kitakura S, Inoue Y, Bednarek P, Schulze-Lefert P, Takano Y. 2017. Dysfunction of Arabidopsis MACPF domain protein activates programmed cell death via tryptophan metabolism in MAMP-triggered immunity. Plant Journal, 89, 381–393.
Gu Y, Zebell S G, Liang Z, Wang S, Kang B H, Dong X. 2016. Nuclear pore permeabilization is a convergent signaling event in effector-triggered immunity. Cell, 166, 1526–1538.
Hamel L P, Sekine K T, Wallon T, Sugiwaka Y, Kobayashi K, Moffett P. 2016. The chloroplastic protein THF1 interacts with the coiled-coil domain of the disease resistance protein N’ and regulates light-dependent cell death. Plant Physiology, 171, 658–674.
Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, Ogasawara K, Nishimura M, Hara-Nishimura I. 2009. A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes and Development, 23, 2496–2506.
Van Hautegem T, Waters A J, Goodrich J, Nowack M K. 2015. Only in dying, life: Programmed cell death during plant development. Trends in Plant Science, 20, 102–113.
Kim S B, Lee H Y, Choi E H, Park E, Kim J H, Moon K B, Kim H S, Choi D. 2018. The coiled-coil and leucine-rich repeat domain of the potyvirus resistance protein Pvr4 has a distinct role in signaling and pathogen recognition. Molecular Plant (Microbe Interaction), 31, 906–913.
Lapin D, Kovacova V, Sun X, Dongus J A, Bhandari D, von Born P, Bautor J, Guarneri N, Rzemieniewski J, Stuttmann J, Beyer A, Parker J E. 2019. A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors. Plant Cell, 31, 2430–2455.
Lee K P, Liu K, Kim E Y, Medina-Puche L, Dong H, Duan J, Li M, Dogra V, Li Y, Lv R, Li Z, Lozano-Duran R, Kim C. 2020. PLANT NATRIURETIC PEPTIDE A and its putative receptor PNP-R2 antagonize salicylic acid-mediated signaling and cell death. Plant Cell, 32, 2237–2250.
Lee M H, Jeon H S, Kim H G, Park O K. 2017. An Arabidopsis NAC transcription factor NAC4 promotes pathogen-induced cell death under negative regulation by microRNA164. New Phytologist, 214, 343–360.
Lema A S, Vercammen D, Serrano I, Valls M, Rivas S, Van Breusegem F, Conlon F L, Dangl J L, Coll N S. 2018. AtSERPIN1 is an inhibitor of the metacaspase AtMC1-mediated cell death and autocatalytic processing in planta. New Phytologist, 218, 1156–1166.
Li B, Sun S, Gao X, Wu M, Deng Y, Zhang Q, Li X, Xiao J, Ke Y, Wang S. 2019. Overexpression a “fruit-weight 22-like” gene OsFWL5 improves rice resistance. Rice (N Y), 12, 51.
Li L, Habring A, Wang K, Weigel D. 2020. Atypical resistance protein RPW8/HR triggers oligomerization of the NLR immune receptor RPP7 and autoimmunity. Cell Host and Microbe, 27, 405–417.
Li W, Ahn IP, Ning Y, Park CH, Zeng L, Whitehill J G, Lu H, Zhao Q, Din, B, Xie Q, Zhou J M, Dai L, Wang G L. 2012. The U-Box/ARM E3 ligase PUB13 regulates cell death, defense, and flowering time in Arabidopsis. Plant Physiology, 159, 239–250.
Li W, Chern M, Yin J, Wang J, Chen X. 2019. Recent advances in broad-spectrum resistance to the rice blast disease. Current Opinion in Plant Biology, 50, 114–120.
Li W, Zhu Z, Chern M, Yin J, Yang C, Ran L, Cheng M, He M, Wang K, Wang J, Zhou X, Zhu X, Chen Z, Wang J, Zhao W, Ma B, Qin P, Chen W, Wang Y, Liu J, et al. 2017. A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell, 170, 114–126.
Li Z, Ding B, Zhou X, Wang G L. 2017. The rice dynamin-related protein OsDRP1E negatively regulates programmed cell death by controlling the release of cytochrome c from Mitochondria. PLoS Pathogens, 13, e1006157.
Li Z, Dogra V, Lee K P, Li R, Li M, Li M, Kim C. 2020. N-terminal acetylation stabilizes SIGMA FACTOR BINDING PROTEIN1 involved in salicylic acid-primed cell death. Plant Physiology, 183, 358–370.
Liang Y, Cui S, Tang X, Zhang Y, Qiu D, Zeng H, Guo L, Yuan J, Yang X. 2018. An asparagine-rich protein Nbnrp1 modulate Verticillium dahliae protein PevD1-induced cell death and disease resistance in Nicotiana benthamiana. Frontiers in Plant Science, 9, 303.
Liu H, Guo Z, Gu F, Ke S, Sun D, Dong S, Liu W, Huang M, Xiao W, Yang G, Liu Y, Guo T, Wang H, Wang J, Chen Z. 2016. 4-Coumarate-CoA ligase-like gene OsAAE3 negatively mediates the rice blast resistance, floret development and lignin biosynthesis. Frontiers in Plant Science, 7, 2041.
Liu H, Ravichandran S, Teh O K, McVey S, Lilley C, Teresinski H J, Gonzalez-Ferrer C, Mullen R, Hofius D, Prithiviraj B, Stone S L. 2017. The RING-type E3 ligase XBAT35.2 is involved in cell death induction and pathogen response. Plant Physiology, 175, 1469–1483.
Liu J, Park C H, He F, Nagano M, Wang M, Bellizzi M, Zhang K, Zeng X, Liu W, Ning Y, Kawano Y, Wang G L. 2015. The RhoGAP SPIN6 associates with SPL11 and OsRac1 and negatively regulates programmed cell death and innate immunity in rice. PLoS Pathogens, 11, e1004629.
Liu P, Guo J, Zhang R, Zhao J, Liu C, Qi T, Duan Y, Kang Z, Guo J. 2019. TaCIPK10 interacts with and phosphorylates TaNH2 to activate wheat defense responses to stripe rust. Plant Biotechnology Journal, 17, 956–968.
Liu Q, Ning Y, Zhang Y, Yu N, Zhao C, Zhan X, Wu W, Chen D, Wei X, Wang G L, Cheng S, Cao L. 2017. OsCUL3a negatively regulates cell death and immunity by degrading OsNPR1 in rice. Plant Cell, 29, 345–359.
Liu Q, Yang J, Zhang S, Zhao J, Feng A, Yang T, Wang X, Mao X, Dong J, Zhu X, Leung H, Leach J E, Liu B. 2016. OsGF14e positively regulates panicle blast resistance in rice. Biochemical and Biophysical Research Communications, 471, 247–252.
Liu X, Liu H, Liu W C, Gao Z. 2020. The nuclear localized RIN13 induces cell death through interacting with ARF1. Biochemcal and Biophysical Research Communications, 527, 124–130.
Ma J, Wang Y, Ma X, Meng L, Jing R, Wang F, Wang S, Cheng Z, Zhang X, Jiang L, Wang J, Wang J, Zhao Z, Guo X, Lin Q, Wu F, Zhu S, Wu C, Ren Y, Lei C, et al. 2019. Disruption of gene SPL35, encoding a novel CUE domain-containing protein, leads to cell death and enhanced disease response in rice. Plant Biotechnology Journal, 17, 1679–1693.
Matsui H, Fujiwara M, Hamada S, Shimamoto K, Nomura Y, Nakagami H, Takahashi A, Hirochika H. 2014. Plasma membrane localization is essential for Oryza sativa Pto-interacting protein 1a-mediated negative regulation of immune signaling in rice. Plant Physiology, 166, 327–336.
Miao Y, Xu L, He X, Zhang L, Shaban M, Zhang X, Zhu L. 2019. Suppression of tryptophan synthase activates cotton immunity by triggering cell death via promoting SA synthesis. Plant Journal, 98, 329–345.
Munch D, Teh O K, Malinovsky F G, Liu Q, Vetukuri R R, Kasmi EI F, Brodersen P, Hara-Nishimura I, Dangl J L, Petersen M, Mundy J, Hofius D. 2015. Retromer contributes to immunity-associated cell death in Arabidopsis. Plant Cell, 27, 463–479.
Nishimura M T, Anderson R G, Cherkis K A, Law T F, Liu Q L, Machius M, Nimchuk Z L, Yang L, Chung E H, Kasmi EI F, Hyunh M, Osborne N E, Sondek J E, Dangl J L. 2017. TIR-only protein RBA1 recognizes a pathogen effector to regulate cell death in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 114, E2053–E2062.
Oh C S, Martin G B, Beer S V. 2007. DspA/E, a type III effector of Erwinia amylovora, is required for early rapid growth in Nicotiana benthamiana and causes NbSGT1 dependent cell death. Molecular Plant Pathology, 8, 255–265.
Oh C S, Pedley K F, Martin G B. 2010. Tomato 14-3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK α. Plant Cell, 22, 260–272.
Park C H, Shirsekar G, Bellizzi M, Chen S, Songkumarn P, Xie X, Shi X, Ning Y, Zhou B, Suttiviriya P, Wang M, Umemura K, Wang G L. 2016. The E3 ligase APIP10 connects the effector AvrPiz-t to the NLR receptor Piz-t in rice. PLoS Pathogens, 12, e1005529.
Park C J, Wei T, Sharma R, Ronald P C. 2017. Overexpression of rice auxilin-like protein, XB21, induces necrotic lesions, up-regulates endocytosis-related genes, and confers enhanced resistance to Xanthomonas oryzae pv oryzae. Rice (N Y), 10, 27.
Pitsili E, Phukan U J, Coll N S. 2020. Cell death in plant immunity. Cold Spring Harbor Perspectives in Biology, 12, 6.
Qiao Y, Jiang W, Lee J, Park B, Choi M S, Piao R, Woo M O, Roh J H, Han L, Paek N C, Seo H S, Koh H J. 2010. SPL28 encodes a clathrin-associated adaptor protein complex 1, medium subunit micro 1 (AP1M1) and is responsible for spotted leaf and early senescence in rice (Oryza sativa). New Phytologist, 185, 258–274.
Qin P, Fan S, Deng L, Zhong G, Zhang S, Li M, Chen W, Wang G, Tu B, Wang Y, Chen X, Ma B, Li S. 2018. LML1, encoding a conserved eukaryotic release factor 1 protein, regulates cell death and pathogen resistance by forming a conserved complex with SPL33 in rice. Plant Cell Physiology, 59, 887–902.
Ruan B, Hua Z, Zhao J, Zhang B, Ren D, Liu C, Yang S, Zhang A, Jiang H, Yu H, Hu J, Zhu L, Chen G, Shen L, Dong G, Zhang G, Zeng D, Guo L, Qian Q, Gao Z. 2019. OsACL-A2 negatively regulates cell death and disease resistance in rice. Plant Biotechnology Journal, 17, 1344–1356.
Schreiber K J, Bentham A, Williams S J, Kobe B, Staskawicz B J. 2016. Multiple domain associations within the Arabidopsis immune receptor RPP1 regulate the activation of programmed cell death. PLoS Pathogens, 12, e1005769.
Shao Z, Zhao Y, Liu L, Chen S, Li C, Meng F, Liu H, Hu S, Wang J, Wang Q. 2020. Overexpression of FBR41 enhances resistance to sphinganine analog mycotoxin-induced cell death and Alternaria stem canker in tomato. Plant Biotechnology Journal, 18, 141–154.
Shirasu K, Nakajima H, Rajasekhar V K, Dixon R A, Lamb C. 1997. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell, 9, 261–270.
de la Torre F, Gutierrez-Beltran E, Pareja-Jaime Y, Chakravarthy S, Martin G B, Del P O. 2013. The tomato calcium sensor Cbl10 and its interacting protein kinase Cipk6 define a signaling pathway in plant immunity. Plant Cell, 25, 2748–2764.
Tu R, Wang H, Liu Q, Wang D, Zhou X, Xu P, Zhang Y, Wu W, Chen D, Cao L, Cheng S, Shen X. 2020. Characterization and genetic analysis of the oshpl3 rice lesion mimic mutant showing spontaneous cell death and enhanced bacterial blight resistance. Plant Physiology and Biochemistry, 154, 94–104.
Vi L R, Kim S K, Mi J, Mariappan K G, Siodmak A, Al-Babili S, Hirt H. 2019. A chimeric IDD4 repressor constitutively induces immunity in Arabidopsis via the modulation of salicylic acid and jasmonic acid homeostasis. Plant Cell Physiology, 60, 1536–1555.
De Vleesschauwer D, Gheysen G, Hofte M. 2013. Hormone defense networking in rice: Tales from a different world. Trends in Plant Science, 18, 10.
Vlot A C, Dempsey D A, Klessig D F. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology, 47, 177–206.
Wang J, Hu M, Wang J, Qi J, Han Z, Wang G, Qi Y, Wang H W, Zhou J M, Chai J. 2019a. A reconstitution and structure of a plant NLR resistosome conferring immunity. Science, 364, 6435.
Wang J, Liu X, Zhang A, Ren Y, Wu F, Wang G, Xu Y, Lei C, Zhu S, Pan T, Wang Y, Zhang H, Wang F, Tan Y Q, Wang Y, Jin X, Luo S, Zhou C, Zhang X, Liu J, et al. 2019b. A cyclic nucleotide-gated channel mediates cytoplasmic calcium elevation and disease resistance in rice. Cell Research, 29, 820–831.
Wang J, Qu B, Dou S, Li L, Yin D, Pang Z, Zhou Z, Tian M, Liu G, Xie Q, Tang D, Chen X, Zhu L. 2015. The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity. BMC Plant Biology, 15, 49.
Wang L, Wen R, Wang J, Xiang D, Wang Q, Zang Y, Wang Z, Huang S, Li X, Datla R, Fobert P R, Wang H, Wei Y, Xiao W. 2019. Arabidopsis UBC13 differentially regulates two programmed cell death pathways in responses to pathogen and low-temperature stress. New Phytologist, 221, 919–934.
Wang Q, Li Y, Ishikawa K, Kosami K I, Uno K, Nagawa S, Tan L, Du J, Shimamoto K, Kawano Y. 2018. Resistance protein Pit interacts with the GEF OsSPK1 to activate OsRac1 and trigger rice immunity. Proceedings of the National Academy of Sciences of the United States of America, 115, E11551–E11560.
Wang R, Ning Y, Shi X, He F, Zhang C, Fan J, Jiang N, Zhang Y, Zhang T, Hu Y, Bellizzi M, Wang G L. 2016. Immunity to rice blast disease by suppression of effector-triggered necrosis. Current Biology, 26, 2399–2411.
Wang S, Gu Y, Zebell S G, Anderson L K, Wang W, Mohan R, Dong X. 2014. A noncanonical role for the CKI-RB-E2F cell-cycle signaling pathway in plant effector-triggered immunity. Cell Host and Microbe, 16, 787–794.
Wang S, Lei C, Wang J, Ma J, Tang S, Wang C, Zhao K, Tian P, Zhang H, Qi C, Cheng Z, Zhang X, Guo X, Liu L, Wu C, Wan J. 2017. SPL33, encoding an eEF1A-like protein, negatively regulates cell death and defense responses in rice. Journal of Experimental Botany, 68, 899–913.
Wang Z, Xia Y, Lin S, Wang Y, Guo B, Song X, Ding S, Zheng L, Feng R, Chen S, Bao Y, Sheng C, Zhang X, Wu J, Niu D, Jin H, Zhao H. 2018. Osa-miR164a targets OsNAC60 and negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Plant Journal, 95, 584–597.
Wierzba M P, Tax F E. 2016. An allelic series of bak1 mutations differentially alter bir1 cell death, immune response, growth, and root development phenotypes in Arabidopsis thaliana. Genetics, 202, 689–702.
Wrzaczek M, Vainonen J P, Stael S, Tsiatsiani L, Help-Rinta-Rahko H, Gauthier A, Kaufholdt D, Bollhoner B, Lamminmaki A, Staes A, Gevaert K, Tuominen H, Van Breusegem F, Helariutta Y, Kangasjarvi J. 2015. GRIM REAPER peptide binds to receptor kinase PRK5 to trigger cell death in Arabidopsis. EMBO Journal, 34, 55–66.
Xu X, Chen Z, Shi Y F, Wang H M, He Y, Shi L, Chen T, Wu J L, Zhang X B. 2018. Functional inactivation of OsGCNT induces enhanced disease resistance to Xanthomonas oryzae pv oryzae in rice. BMC Plant Biology, 18, 264.
Yadeta K A, Elmore J M, Creer A Y, Feng B, Franco J Y, Rufian J S, He P, Phinney B, Coaker G. 2017. A cysteine-rich protein kinase associates with a membrane immune complex and the cysteine residues are required for cell death. Plant Physiology, 173, 771–787.
Yang D L, Yang Y, He Z. 2013. Roles of plant hormones and their interplay in rice immunity. Molecular Plant, 6, 675–685.
You Q, Zhai K, Yang D, Yang W, Wu J, Liu J, Pan W, Wang J, Zhu X, Jian Y, Liu J, Zhang Y, Deng Y, Li Q, Lou Y, Xie Q, He Z. 2016. An E3 ubiquitin ligase-BAG protein module controls plant innate immunity and broad-spectrum disease resistance. Cell Host and Microbe, 20, 758–769.
Yuan M, Jiang Z, Bi G, Nomura K, Liu M, Wang Y, Cai B, Zhou J M, He S Y, Xin X F. 2021. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature, 592, 105–109.
Zhang D, Liu M, Tang M, Dong B, Wu D, Zhang Z, Zhou B. 2015. Repression of microRNA biogenesis by silencing of OsDCL1 activates the basal resistance to Magnaporthe oryzae in rice. Plant Science, 237, 24–32.
Zhang H, Li D, Wang M, Liu J, Teng W, Cheng B, Huang Q, Wang M, Song W, Dong S, Zheng X, Zhang Z. 2012. The Nicotiana benthamiana mitogen-activated protein kinase cascade and WRKY transcription factor participate in Nep1(Mo)-triggered plant responses. Molecular Plant (Microbe Interaction), 25, 1639–1653.
Zhang Y, Liu Q, Zhang Y, Chen Y, Yu N, Cao Y, Zhan X, Cheng S, Cao L. 2019. LMM24 encodes receptor-like cytoplasmic kinase 109, which regulates cell death and defense responses in rice. International Journal of Molecular Sciences, 20, 13.
Zhao J, Liu P, Li C, Wang Y, Guo L, Jiang G, Zhai W. 2017. LMM5.1 and LMM5.4, two eukaryotic translation elongation factor 1A-like gene family members, negatively affect cell death and disease resistance in rice. Journal of Genetics and Genomics, 44, 107–118.
Zhao Z X, Feng Q, Liu P Q, He X R, Zhao J H, Xu Y J, Zhang L L, Huang Y Y, Zhao J Q, Fan J, Li Y, Xiao S, Wang W M. 2020. RPW81 enhances the ethylene-signaling pathway to feedback-attenuate its mediated cell death and disease resistance in Arabidopsis. New Phytologist, 229, 516–531.
Zeng L, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm B H, Leung H, Wang G L. 2004. Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-Box/Armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell, 16, 2795–2808.
Zhu X, Yin J, Liang S, Liang R, Zhou X, Chen Z, Zhao W, Wang J, Li W, He M, Yuan C, Miyamoto K, Ma B, Wang J, Qin P, Chen W, Wang Y, Wang W, Wu X, Yamane H, et al. 2016. The multivesicular bodies (MVBs)-localized AAA ATPase LRD6-6 inhibits immunity and cell death likely through regulating MVBs-mediated vesicular trafficking in rice. PLoS Genetics, 12, e1006311.
|
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
