Bacterial blight; Cell wall; Leaf tip necrosis; Polygalacturonase; Rice; Agronomy and Crop Science; Soil Science; Plant Science
Abstract :
[en] [en] BACKGROUND: Plant cell walls are the main physical barrier encountered by pathogens colonizing plant tissues. Alteration of cell wall integrity (CWI) can activate specific defenses by impairing proteins involved in cell wall biosynthesis, degradation and remodeling, or cell wall damage due to biotic or abiotic stress. Polygalacturonase (PG) depolymerize pectin by hydrolysis, thereby altering pectin composition and structures and activating cell wall defense. Although many studies of CWI have been reported, the mechanism of how PGs regulate cell wall immune response is not well understood.
RESULTS: Necrosis appeared in leaf tips at the tillering stage, finally resulting in 3-5 cm of dark brown necrotic tissue. ltn-212 showed obvious cell death and accumulation of H2O2 in leaf tips. The defense responses were activated in ltn-212 to resist bacterial blight pathogen of rice. Map based cloning revealed that a single base substitution (G-A) in the first intron caused incorrect splicing of OsPG1, resulting in a necrotic phenotype. OsPG1 is constitutively expressed in all organs, and the wild-type phenotype was restored in complementation individuals and knockout of wild-type lines resulted in necrosis as in ltn-212. Transmission electron microscopy showed that thicknesses of cell walls were significantly reduced and cell size and shape were significantly diminished in ltn-212.
CONCLUSION: These results demonstrate that OsPG1 encodes a PG in response to the leaf tip necrosis phenotype of ltn-212. Loss-of-function mutation of ltn-212 destroyed CWI, resulting in spontaneous cell death and an auto-activated defense response including reactive oxygen species (ROS) burst and pathogenesis-related (PR) gene expression, as well as enhanced resistance to Xanthomonas oryzae pv. oryzae (Xoo). These findings promote our understanding of the CWI mediated defense response.
Cao, Yongrun; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China
Zhang, Yue ; Université de Liège - ULiège > TERRA Research Centre ; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China
Chen, Yuyu; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China
Yu, Ning; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China
Liaqat, Shah; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China
Wu, Weixun; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China
Chen, Daibo; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China
Cheng, Shihua; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China
Wei, Xinghua; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China
Cao, Liyong; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China
Zhang, Yingxin; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China. zhangyingxin@caas.cn ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China. zhangyingxin@caas.cn
Liu, Qunen ; State Key Laboratory of Rice Biology, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China. liuqunen202@163.com ; Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Zhejiang, 310006, Hangzhou, China. liuqunen202@163.com
Language :
English
Title :
OsPG1 Encodes a Polygalacturonase that Determines Cell Wall Architecture and Affects Resistance to Bacterial Blight Pathogen in Rice.
NSCF - National Natural Science Foundation of China CAAS - Chinese Academy of Agricultural Sciences
Funding text :
We thank Quanzhi Zhao, Junzhou Li (Henan Agricultural University) for providing opportunity to study at CNRRI. We also thank Bio-Ultrastructure Analysis Lab. of Analysis Center of Agrobiology and Environmental Sciences, Zhejiang Univ. for TEM observation.National Natural Science Foundation of China (31801726, 31871236, and 31521064), the National Key Transgenic Program (2016ZX08001002), and the Agricultural Science and Technology Innovation Program of the Chinese Academy of the Agricultural Sciences (CAAS-ASTIP-2013-CNRRI). the Fundamental Research Funds of Central Public Welfare Research Institutions (2017RG001–1).
Annis SL, Goodwin PH (1997) Recent advances in the molecular genetics of plant cell wall-degrading enzymes produced by plant pathogenic fungi. Eur J Plant Pathol 103(1):1–14. 10.1023/A:1008656013255 DOI: 10.1023/A:1008656013255
Atkinson RG, Schroder R, Hallett IC, Cohen D, MacRae EA (2002) Overexpression of Polygalacturonase in transgenic apple trees leads to a range of novel phenotypes involving changes in cell adhesion. Plant Physiol 129(1):122–133. 10.1104/pp.010986 DOI: 10.1104/pp.010986
Atmodjo MA, Hao ZY, Mohnen D (2013) Evolving views of pectin biosynthesis. Annu Rev Plant Biol 64(1):747–779. 10.1146/annurev-arplant-042811-105534 DOI: 10.1146/annurev-arplant-042811-105534
Bellincampi D, Cervone F, Lionetti V (2014) Plant cell wall dynamics and wall-related susceptibility in plant–pathogen interactions. Front Plant Sci 5:228–228 DOI: 10.3389/fpls.2014.00228
Bonnin E, Garnier C, Ralet M (2014) Pectin-modifying enzymes and pectin-derived materials: applications and impacts. Applied microbiology. Biotechnology 98:519–532
Cantu D, Vicente AR, Labavitch JM, Bennett AB, Powell ALT (2008) Strangers in the matrix: plant cell walls and pathogen susceptibility. Trends Plant Sci 13(11):610–617. 10.1016/j.tplants.2008.09.002 DOI: 10.1016/j.tplants.2008.09.002
Engelsdorf T, Will C, Hofmann J, Schmitt C, Merritt BB, Rieger L, Frenger MS, Marschall A, Franke R, Pattathil S (2016) Cell wall composition and penetration resistance against the fungal pathogen Colletotrichum higginsianum are affected by impaired starch turnover in Arabidopsis mutants. J Exp Bot 68:701–713
Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D, Cervone F, De LG (2007) Transgenic expression of a fungal endo-Polygalacturonase increases plant resistance to pathogens and reduces Auxin sensitivity. Plant Physiol 146:669–681
Gallegogiraldo L, Liu C, Posealbacete S, Pattathil S, Peralta AG, Young J, Westpheling J, Hahn MG, Rao XL, Knox JP, Knox JP, Meester BD, Boerjan W, Dixon RA (2020) ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE 1 (ADPG1) releases latent defense signals in stems with reduced lignin content. Proc Natl Acad Sci U S A 117(6):3281–3290. 10.1073/pnas.1914422117 DOI: 10.1073/pnas.1914422117
Gunawardena AH, Greenwood JS, Dengler NG (2007) Cell wall degradation and modification during programmed cell death in lace plant, APONOGETON MADAGASCARIENSIS (APONOGETONACEAE). Am J Bot 94(7):1116–1128. 10.3732/ajb.94.7.1116 DOI: 10.3732/ajb.94.7.1116
Hadfield KA, Bennett AB (1998) Polygalacturonases: many genes in search of a function. Plant Physiol 117(2):337–343. 10.1104/pp.117.2.337 DOI: 10.1104/pp.117.2.337
He YJ, Karre S, Johal GS, Christensen SA, Balint-Kurti P (2019) A maize polygalacturonase functions as a suppressor of programmed cell death in plants. BMC Plant Biol 19(1):310. 10.1186/s12870-019-1897-5 DOI: 10.1186/s12870-019-1897-5
Hong YB, Zhang YX, Sinumporn S, Yu N, Xd Z, Shen XH, Chen DB, Yu P, Wu WX, Liu QE, Cao ZY, Zhao CD, Cheng SH, Cao LY (2018) Premature leaf senescence 3, encoding a methyltransferase, is required for melatonin biosynthesis in rice. Plant J 95(5):877–891. 10.1111/tpj.13995 DOI: 10.1111/tpj.13995
Hongo S, Sato K, Yokoyama R, Nishitani K (2012) Demethylesterification of the primary wall by PECTIN METHYLESTERASE35 provides mechanical support to the Arabidopsis stem. Plant Cell 24(6):2624–2634. 10.1105/tpc.112.099325 DOI: 10.1105/tpc.112.099325
Hu B, Zhu CG, Li F, Tang JY, Wang YQ, Lin AH, Liu LC, Che RH, Chu CC (2011) LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol 156(3):1101–1115. 10.1104/pp.110.170209 DOI: 10.1104/pp.110.170209
Itoh J, Nonomura K, Ikeda K, So Y, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development from zygote to spikelet. Plant Physiology Cell 46(1):23–47. 10.1093/pcp/pci501 DOI: 10.1093/pcp/pci501
Jia HF, Ren HY, Gu M, Zhao JN, Sun SB, Zhang X, Chen JY, Wu P, Xu GH (2011) The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in Rice. Plant Physiol 156(3):1164–1175. 10.1104/pp.111.175240 DOI: 10.1104/pp.111.175240
Kesten C, Menna A, Sanchezrodriguez C (2017) Regulation of cellulose synthesis in response to stress. Curr Opin Plant Biol 40:106–113. 10.1016/j.pbi.2017.08.010 DOI: 10.1016/j.pbi.2017.08.010
Kim J, Shiu S, Thoma S, Li W, Patterson SE (2006) Patterns of expansion and expression divergence in the plant polygalacturonase gene family. Genome Biol 7:1–14
Krattinger SG, Sucher J, Selter LL, Chauhan H, Zhou B, Tang MZ, Upadhyaya NM, Mieulet D, Guiderdoni E, Weidenbach D, Schaffrath U, Lagudah ES, Keller B (2016) The wheat durable, multipathogen resistance gene Lr34 confers partial blast resistance in rice. Plant Biotechnol J 14(5):1261–1268. 10.1111/pbi.12491 DOI: 10.1111/pbi.12491
Leng YJ, Yang YL, Ren DY, Huang LC, Dai LP, Wang YQ, Chen L, Tu ZJ, Gao YH, Li XY, Zhu L, Hu J, Zhang GH, Gao ZY, Guo LB, Kong ZS, Lin YJ, Qian Q, Zeng DL (2017) A Rice PECTATE LYASE-LIKE gene is required for plant growth and leaf senescence. Plant Physiol 174(2):1151–1166. 10.1104/pp.16.01625 DOI: 10.1104/pp.16.01625
Li JG, Zhu H, Yuan RC (2010) Profiling the expression of genes related to ethylene biosynthesis, ethylene perception, and cell wall degradation during fruit abscission and fruit ripening in apple. J Am Soc Hortic Sci 135(5):391–401. 10.21273/JASHS.135.5.391 DOI: 10.21273/JASHS.135.5.391
Lionetti V, Fabri E, De CM, Hansen AR, Willats WGT, Piro G, Bellincampi D (2017) Three pectin Methylesterase inhibitors protect Cell Wall integrity for Arabidopsis immunity to Botrytis. Plant Physiol 173(3):1844–1863. 10.1104/pp.16.01185 DOI: 10.1104/pp.16.01185
Liu H, Ma Y, Chen NA, Guo SY, Liu HL, Guo XY, Chong K, Xu YY (2014) Overexpression of stress-inducible OsBURP16, the β subunit of polygalacturonase 1, decreases pectin content and cell adhesion and increases abiotic stress sensitivity in rice. Plant Cell Environ 37(5):1144–1158. 10.1111/pce.12223 DOI: 10.1111/pce.12223
Liu H, Wang Y, Xu J, Su T, Liu G, Ren D (2008) Ethylene Signaling is required for the acceleration of cell death induced by the activation of AtMEK5 in Arabidopsis. Cell Res 18:422-432. 10.1038/cr.2008.2. DOI: 10.1038/cr.2008.29
Liu Hk, Qian M, Song CH, Li JJ, Zhao CP, Li GF, Wang AZ, Han MY (2018) Down-Regulation of PpBGAL10 and PpBGAL16 Delays Fruit Softening in Peach by Reducing Polygalacturonase and Pectin Methylesterase Activity. Frontiers in Plant Science 9:1015.
Liu QE, Ning YS, Zhang YX, Yu N, Zhao CD, Zhan XD, Wu WX, Chen DB, Wei XJ, Wang GL, Cheng SH, Cao LY (2017) OsCUL3a Negatively Regulates Cell Death and Immunity by Degrading OsNPR1 in Rice. Plant Cell. 29:345–359. 10.1105/tpc.16.00650. DOI: 10.1105/tpc.16.00650
Ma J, Wang YF, Ma XD, Meng LZ, Jing RN, Wang F, Wang S, Cheng ZJ, Zhang X, Jiang L, Zhao ZC, Guo XP, Lin QB, Wu FQ, Zhu SS, Wu CY, Ren YL, Lei CL, Zhai HQ, Wan JM (2019) Disruption of gene SPL35, encoding a novel CUE domain-containing protein, leads to cell death and enhanced disease response in rice. Plant Biotechnol J 17(8):1679–1693. 10.1111/pbi.13093 DOI: 10.1111/pbi.13093
Malinovsky FG, Fangel JU, Willats WGT (2014) The role of the cell wall in plant immunity. Front Plant Sci 5:178–178 DOI: 10.3389/fpls.2014.00178
Markovic O, Janecek S (2001) Pectin degrading glycoside hydrolases of family 28: sequence-structural features, specificities and evolution. Protein Eng 14(9):615–631. 10.1093/protein/14.9.615 DOI: 10.1093/protein/14.9.615
Mccarthy TW, Der JP, Honaas LA, Depamphilis CW, Anderson CT (2014) Phylogenetic analysis of pectin-related gene families in Physcomitrella patens and nine other plant species yields evolutionary insights into cell walls. BMC Plant Biol 14(1):79–79. 10.1186/1471-2229-14-79 DOI: 10.1186/1471-2229-14-79
Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6(9):414–419. 10.1016/S1360-1385(01)02045-3 DOI: 10.1016/S1360-1385(01)02045-3
Miedes E, Vanholme R, Boerjan W, Molina A (2014) The role of the secondary Cell Wall in plant resistance to pathogens. Front Plant Sci 5:358–358 DOI: 10.3389/fpls.2014.00358
Ogawa M, Kay P, Wilson S, Swain SM (2009) ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21(1):216–233. 10.1105/tpc.108.063768 DOI: 10.1105/tpc.108.063768
Peaucelle A, Braybrook SA, Hofte H (2012) Cell wall mechanics and growth control in plants: the role of pectins revisited. Front Plant Sci 3:121–121 DOI: 10.3389/fpls.2012.00121
Quesada MA, Blancoportales R, Pose S, Garciagago JA, Jimenezbermudez S, Munozserrano A, Caballero JL, Pliegoalfaro F, Mercado JA, Munozblanco J (2009) Antisense Down-regulation of the FaPG1 gene reveals an unexpected central role for Polygalacturonase in strawberry fruit softening. Plant Physiol 150(2):1022–1032. 10.1104/pp.109.138297 DOI: 10.1104/pp.109.138297
Rani MH, Liu QE, Yu N, Zhang YX, Wang BF, Cao YR, Zhang Y, Islam A, Anley ZW, Cao Liyong Cheng SH (2020) ES5 is involved in the regulation of phosphatidylserine synthesis and impacts on early senescence in rice (Oryza sativa L). Plant Mol Biol 102(4-5):501–515. https://doi.org/10.1007/s11103-019-00961-4
Rhee SY, Osborne E, Poindexter PD, Somerville CR (2003) Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiol 133(3):1170–1180. 10.1104/pp.103.028266 DOI: 10.1104/pp.103.028266
Risk JM, Selter LL, Chauhan H, Krattinger SG, Kumlehn J, Hensel G, Viccars L, Richardson T, Buesing G, Troller A, Lagudah ES, Beat K (2013) The wheat Lr34 gene provides resistance against multiple fungal pathogens in barley. Plant Biotechnol J 11(7):847–854. 10.1111/pbi.12077 DOI: 10.1111/pbi.12077
Ruan BP, Hua ZH, Zhao J, Zhang B, Ren DY, Liu CL, Yang SL, Zhang AP, Jiang HZ, Yu HP, Hu J, Zhu L, Chen G, Shen L, Dong GJ, Zhang GH, Zeng DL, Guo LB, Qian Q, Gao ZY (2019) OsACL-A2 negatively regulates cell death and disease resistance in rice. Plant Biotechnol J 17(7):1344–1356. 10.1111/pbi.13058 DOI: 10.1111/pbi.13058
Rui Y, Xiao CW, Yi H, Kandemir B, Wang JZ, Puri VM, Anderson CT (2017) POLYGALACTURONASE INVOLVED IN EXPANSION3 functions in seedling development, rosette growth, and Stomatal dynamics in Arabidopsis thaliana. Plant Cell 29(10):2413–2432. 10.1105/tpc.17.00568 DOI: 10.1105/tpc.17.00568
Sarkar P, Bosneaga E, Auer M (2009) Plant cell walls throughout evolution: towards a molecular understanding of their design principles. J Exp Bot 60(13):3615–3635. 10.1093/jxb/erp245 DOI: 10.1093/jxb/erp245
Sathe AP, Su XN, Chen Z, Chen T, Wei XJ, Tang SQ, Zhang XB, Wu JL (2019) Identification and characterization of a spotted-leaf mutant spl40 with enhanced bacterial blight resistance in rice. Rice 12:1–15 DOI: 10.1186/s12284-019-0326-6
Singh RP (1992) Association between gene Lr34 for leaf rust resistance and leaf tip necrosis in wheat. Crop Sci 32(4):874–878. 10.2135/cropsci1992.0011183X003200040008x DOI: 10.2135/cropsci1992.0011183X003200040008x
Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H (2004) Toward a systems approach to understanding plant-cell walls. Science 306(5705):2206–2211. 10.1126/science.1102765 DOI: 10.1126/science.1102765
Van BF, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390 DOI: 10.1104/pp.106.078295
Villarreal NM, Martínez GA, Civello PM (2009) Influence of plant growth regulators on polygalacturonase expression in strawberry fruit. Chin Academy Agric Sci 176:0–757
Vogel JP, Raab TK, Schiff C, Somerville SC (2002) PMR6, a Pectate Lyase–like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell 14(9):2095–2106. 10.1105/tpc.003509 DOI: 10.1105/tpc.003509
Wakasa Y, Kudo H, Ishikawa R, Akada S, Senda M, Niizeki M, Harada T (2006) Low expression of an endopolygalacturonase gene in apple fruit with long-term storage potential. Technol Postharvest Biol 39(2):193–198. 10.1016/j.postharvbio.2005.10.005 DOI: 10.1016/j.postharvbio.2005.10.005
Wang X, Hou SG, Wu QQ, Lin MY, Acharya BR, Wu DJ, Zhang W (2017) IDL6-HAE/HSL2 impacts pectin degradation and resistance to Pseudomonas syringae pv tomato DC3000 in Arabidopsis leaves. Plant J 89(2):250–263. 10.1111/tpj.13380 DOI: 10.1111/tpj.13380
Wang YQ, Wan ZY, CAO JS, YU Xiao-Lin, XIANG X, LU G (2005) Cloning and characterization of the microspore development-related gene BcMF2 in Chinese cabbage Pak-Choi (Brassica campestris L. ssp. chinensis Makino). J Integr Plant Biol, 47: 863–872, 7, DOI: https://doi.org/10.1111/j.1744-7909.2005.00101.x
Wolf S, Gregory M, Jerome P (2009) Homogalacturonan methyl-esterification and plant development. Mol Plant 2(5):851–860. 10.1093/mp/ssp066 DOI: 10.1093/mp/ssp066
Wu LW, Ren DY, Hu SK, Li GG, Dong GJ, Jiang L, Hu XM, Ye WJ, Cui YT, Zhu L, Hu J, Zhang GH, Gao ZY, Zeng DL, Qian Q, Guo LB (2016) Down-regulation of a Nicotinate Phosphoribosyltransferase gene, OsNaPRT1, leads to withered leaf tips. Plant Physiol 171(2):1085–1098. 10.1104/pp.15.01898 DOI: 10.1104/pp.15.01898
Xiao CW, Barnes WJ, Zamil MS, Yi H, Puri VM, Anderson CT (2017) Activation tagging of Arabidopsis POLYGALACTURONASE INVOLVED IN EXPANSION2 promotes hypocotyl elongation, leaf EXPANSION, stem lignification, mechanical stiffening, and lodging. Plant J 89(6):1159–1173. 10.1111/tpj.13453 DOI: 10.1111/tpj.13453
Xiao CW, Somerville C, Anderson CT (2014) POLYGALACTURONASE INVOLVED IN EXPANSION1 functions in cell elongation and flower development in Arabidopsis. Plant Cell 26(3):1018–1035. 10.1105/tpc.114.123968 DOI: 10.1105/tpc.114.123968
Zurbriggen MD, Carrillo N, Hajirezaei M (2010) ROS signaling in the hypersensitive response: when, where and what for? Plant Signal Behav 5(4):393–396. 10.4161/psb.5.4.10793 DOI: 10.4161/psb.5.4.10793
