Scientia Agricultura Sinica ›› 2023, Vol. 56 ›› Issue (5): 879-891.doi: 10.3864/j.issn.0578-1752.2023.05.006

• PLANT PROTECTION • Previous Articles     Next Articles

Expression and Functional Analysis of Glycosyl Hydrolase Genes from Plasmopara viticola

PAN FengYing(), QU JunJie, LIU LuLu, SUN DaYun, GUO ZeXi, WEI XiaoLi, WEI ShuMei, YIN Ling()   

  1. Key Lab of Guangxi Crop Genetic Improvement and Biotechnology, Guangxi Academy of Agricultural Sciences, Nanning 530007
  • Received:2022-10-21 Accepted:2022-11-24 Online:2023-03-01 Published:2023-03-13

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Abstract:

【Objective】The objective of this study is to clone glycosyl hydrolase genes from Plasmopara viticola (PvGHs), analyze their characteristics and expression patterns in infected grape leaves, and the abilities to inhibit or promote programmed cell death (PCD) and affect Phytophthora nicotianae infection in tobacco leaves, so as to provide a theoretical basis for further study on mechanism of regulating host plant immunity.【Method】Eight PvGHs with full-length were amplified by RT-PCR from P. viticola Pv5-27 strain. The sequences of these eight PvGHs and encoded proteins were analyzed by bioinformatics. Yeast signal peptide trap system (SST) was used to verify the secretory activity of the PvGH proteins. The expression pattern of PvGHs during infection grape leaves was detected by qRT-PCR. At the same time, eight PvGH effector proteins were transiently expressed in Nicotiana benthamiana by Agrobacterium-mediated PVX virus expression system. Moreover, their inhibitory abilities to inhibit INF1- and BAX-triggered PCD and to promote P. nicotianae infection were also analyzed.【Result】The sequences of eight PvGHs were completely consistent with the prediction in genome sequence, with the length of 1 092 to 1 392 bp, encoding 364-464 amino acids, respectively. The similarity with homologous proteins from other oomycetes was as high as 60.62%-86.36%. None of them had transmembrane domains. Their secondary structures were quite different from each other, and their tertiary structures were less similar to those of other proteins, which showed a very unique tertiary structure. SingalP 5.0 software was used to predict signal peptide of these proteins. It was found that all the PvGH proteins contained signal peptide sequences of 20-26 aa in length. However, the SST verification results showed that PvG09279 and PvG13517 do not have secretion activity. The retention, deletion or replacement of signal peptide sequences of the eight PvGH proteins could inhibit the BAX-triggered PCD and all these PvGH proteins could promote P. nicotianae infection in tobacco leaves. It suggests that the potential virulence of eight PvGH effectors does not dependent on the signal peptide. The up-regulated expression of PvGHs in the early stage of infection of P. viticola further indicated that PvGHs play an important role in the interaction between pathogen and host.【Conclusion】During downy mildew infection, PvGHs secreted by P. viticola are involved in pathogenic process by inhibiting the host PTI response.

Key words: Plasmopara viticola, glycosyl hydrolase, bioinformatics, function analysis

Table 1

The primers used in this study"

引物Primer 序列Sequence (5′-3′) 用途Purpose
pSUC2-G11117F GGATCTTCCAGAGATGAATTCATGACCAAGACATTGCATTCGG 扩增PvG11117信号肽序列
To amplify signal peptide sequence of PvG11117
pSUC2-G11117R CTGCCGTTCGACGATCTCGAGCGCATCAACGCTGAGAGTAGAC
G11117ClaⅠF TCAGCACCAGCTAGCATCGATATGACCAAGACATTGCATTCGG 扩增PvG11117保留或剔除信号肽和替换为PR1信号肽的片段
To amplify fragments of PvG11117 with or without signal peptide and the fragment that replaces PvG11117 signal peptide with PR1 signal peptide
G11117ClaⅠNSPF TCAGCACCAGCTAGCATCGATATGGACAAGTTATGTTCCATTCCG
G11117ClaⅠPR1F TCAGCACCAGCTAGCATCGATATGGGATTTGTTCTCTTTTCGCA
G11117SalⅠR AACCGTTCATCGGCGGTCGACCTAAAACTGGGTGATAGGGGCC
pSUC2-G13516F GGATCTTCCAGAGATGAATTCATGGTGAACGTCCTGTGTGCG 扩增PvG13516信号肽
To amplify signal peptide of PvG13516
pSUC2-G13516R CTGCCGTTCGACGATCTCGAGGGCATCAGCAGAACCGACG
G13516ClaⅠF TCAGCACCAGCTAGCATCGATATGGTGAACGTCCTGTGTGCG 扩增PvG13516保留或剔除信号肽和替换为PR1信号肽的片段
To amplify fragments of PvG13516 with or without signal peptide and the fragment that replaces PvG13516 signal peptide with PR1 signal peptide
G13516ClaⅠNSPF TCAGCACCAGCTAGCATCGATATGAGTCTGTTTAAGTGCTCGGG
G13516ClaⅠPR1F TCAGCACCAGCTAGCATCGATATGGGATTTGTTCTCTTTTCGCA
G13516SalⅠR AACCGTTCATCGGCGGTCGACTTACATGGCGCAGTTCTTGTGC
引物Primer 序列Sequence (5′-3′) 用途Purpose
pSUC2-G10113F GGATCTTCCAGAGATGAATTCATGGTTGCCAACTCGTTGCG 扩增PvG10113信号肽
To amplify signal peptide of PvG10113
pSUC2-G10113R CTGCCGTTCGACGATCTCGAGAACAATTGATGATAAAAAGAGTGCAAC
G10113ClaⅠF TCAGCACCAGCTAGCATCGATATGGTTGCCAACTCGTTGCG 扩增PvG10113保留或剔除信号肽和替换为PR1信号肽的片段
To amplify fragments of PvG10113 with or without signal peptide and the fragment that replaces PvG10113 signal peptide with PR1 signal peptide
G10113ClaⅠNSPF TCAGCACCAGCTAGCATCGATATGGCCGAAGACCTGTGCT
G10113ClaⅠPR1F TCAGCACCAGCTAGCATCGATATGGGATTTGTTCTCTTTTCGCA
G10113SalⅠR AACCGTTCATCGGCGGTCGACTTACTGCAAGAATTGCTTTCTTACTCG
pSUC2-G01792F GGATCTTCCAGAGATGAATTCATGTTTCGCGAAGTTGCTTTCT 扩增PvG01792信号肽
To amplify signal peptide of PvG01792
pSUC2-G01792R CTGCCGTTCGACGATCTCGAGCGCTAAAGTCGAAGACCCTAACA
G01792ClaⅠF TCAGCACCAGCTAGCATCGATATGTTTCGCGAAGTTGCTTTCT 扩增PvG01792保留或剔除信号肽和替换为PR1信号肽的片段
To amplify fragments of PvG01792 with or without signal peptide and the fragment that replaces PvG01792 signal peptide with PR1 signal peptide
G01792ClaⅠNSPF TCAGCACCAGCTAGCATCGATATGCTGGATCAGAAGCTGTATGG
G01792ClaⅠPR1F TCAGCACCAGCTAGCATCGATATGGGATTTGTTCTCTTTTCGCA
G01792SalⅠR AACCGTTCATCGGCGGTCGACTTACAAATACCAGAAAACGGTGGA
pSUC2-G09279F GGATCTTCCAGAGATGAATTCATGCAGCTTCTTTTTACTGCAATC 扩增PvG09279信号肽
To amplify signal peptide of PvG09279
pSUC2-G09279R CTGCCGTTCGACGATCTCGAGACTCTCAATCGTCATCATGAGCAG
G09279ClaⅠF TCAGCACCAGCTAGCATCGATATGCAGCTTCTTTTTACTGCAATC 扩增PvG09279保留或剔除信号肽和替换为PR1信号肽的片段
To amplify fragments of PvG09279 with or without signal peptide and the fragment that replaces PvG9279 signal peptide with PR1 signal peptide
G09279ClaⅠNSPF TCAGCACCAGCTAGCATCGATATGTCCCAAACGCTTCACCA
G09279ClaⅠPR1F TCAGCACCAGCTAGCATCGATATGGGATTTGTTCTCTTTTCGCA
G09279SalⅠR AACCGTTCATCGGCGGTCGACCTAGAGAGATATGCCAGGGGGA
pSUC2-G02199F GGATCTTCCAGAGATGAATTCATGAAGCTCTCTTCCTCTTTATCCC 扩增PvG02199信号肽
To amplify signal peptide of PvG02199
pSUC2-G02199R CTGCCGTTCGACGATCTCGAGAGCTGATAAAAGGGACGACGAC
G02199ClaⅠF TCAGCACCAGCTAGCATCGATATGAAGCTCTCTTCCTCTTTATCCC 扩增PvG02199保留或剔除信号肽和替换为PR1信号肽的片段
To amplify fragments of PvG02199 with or without signal peptide and the fragment that replaces PvG02199 signal peptide with PR1 signal peptide
G02199ClaⅠNSPF TCAGCACCAGCTAGCATCGATATGCAGCAGATTGGAACGAATA
G02199ClaⅠPR1F TCAGCACCAGCTAGCATCGATATGGGATTTGTTCTCTTTTCGCA
G02199SalⅠR AACCGTTCATCGGCGGTCGACTCAGTACGTGGTTCCGATGTCG
pSUC2-G13517F GGATCTTCCAGAGATGAATTCATGCTATCCTCCAAACTCCTCG 扩增PvG13517信号肽
To amplify signal peptide of PvG13517
pSUC2-G13517R CTGCCGTTCGACGATCTCGAGTCCCGCCGCTTTTTTGCC
G13517ClaⅠF TCAGCACCAGCTAGCATCGATATGCTATCCTCCAAACTCCTCG 扩增PvG13517保留或剔除信号肽和替换为PR1信号肽的片段
To amplify fragments of PvG13517 with or without signal peptide and the fragment that replaces PvG013517 signal peptide with PR1 signal peptide
G13517ClaⅠNSPF TCAGCACCAGCTAGCATCGATATGCAGAATTTTTGTATCCATGGC
G13517ClaⅠPR1F TCAGCACCAGCTAGCATCGATATGGGATTTGTTCTCTTTTCGCA
G13517SalⅠR AACCGTTCATCGGCGGTCGACTTACATGCTTGTTTGGCACTCTTC
pSUC2-G13010F GGATCTTCCAGAGATGAATTCATGTTGCCAGCTTTGCTGTTT 扩增PvG13010信号肽
To amplify signal peptide of PvG13010
pSUC2-G13010R CTGCCGTTCGACGATCTCGAGAGCGCCAATTCCGTCAGTG
G13010ClaⅠF TCAGCACCAGCTAGCATCGATATGTTGCCAGCTTTGCTGTTT 扩增PvG13010保留或剔除信号肽和替换为PR1信号肽的片段
To amplify fragments of PvG13010 with or without signal peptide and the fragment that replaces PvG13010 signal peptide with PR1 signal peptide
G13010ClaⅠNSPF TCAGCACCAGCTAGCATCGATATGGTCGCTGTCGATACGCT
G13010ClaⅠPR1F TCAGCACCAGCTAGCATCGATATGGGATTTGTTCTCTTTTCGCA
G13010SalⅠR AACCGTTCATCGGCGGTCGACCTAAACCTGAAAAAGCACTAATGCC

Fig. 1

PCR products of PvGHs 1: PvG11117; 2: PvG13516; 3: PvG10113; 4: PvG01792; 5: PvG09279; 6: PvG02199; 7: PvG13517; 8: PvG13010"

Table 2

Sequence features of PvGHs and encoded proteins"

基因号
Gene ID		 长度
Length (bp)		 氨基酸
Amino acid
(aa)		 NCBI保守
结构域
Conserved domain		 区间
Interval (aa)		 PFam保守
结构域
Conserved
domain		 区间
Interval
(aa)		 同源蛋白
<BOLD>H</BOLD>omologous
protein		 相似度
<BOLD>S</BOLD>imilarity (%)		 信号肽
Signal peptide (aa)
PvG11117 1131 377 Glyco_hydro_6 super family 44-297 Glycosyl hydrolases family 6 35-300 GH family 6 protein (P. infestans) (KAF4028604.1) 60.62 1-25
PvG13516 1221 407 Glyco_hydro super family 20-300 Glycosyl hydrolases family 17 196-311 Glucan 1,3-beta-D-glucosidase
(P. cinamomi) (CAJ90910.1)		 72.90 1-23
PvG10113 1179 393 Glyco_hydro_6 super family
Cell division protein DedD		 46-295
331-380		 Glycosyl hydrolases family 6 33-301 1,4-cellobiohydrolase (P. cactorum) (KAF1773299.1) 73.83 1-26
PvG01792 1170 390 Glyco_hydro super family 6-289 Glycosyl hydrolases family 17 203-300 GH family 17 protein (P. infestans) (KAF4032687.1) 72.92 1-21
PvG09279 1158 386 Glyco_hydro_28 super family 72-373 Glycosyl hydrolases family 28 72-380 Polygalacturonase (P. cinamomi) (KAG6616063.1) 61.04 1-20
PvG02199 1392 464 GH7_CBH_EG super family 26-462
 Glycosyl hydrolase family 7 26-463 GH family 7 protein (P. infestans) (KAF4031525.1) 86.36 1-23
PvG13517 1092 364 Glyco_hydro super family 1-320 Glycosyl hydrolases family 17 31-309 GH family 3 protein (P. pseudosyringae) (KAG7379682.1) 76.62 1-24
PvG13010 1092 364 Glyco_hydro_6 super family 55-300 Glycosyl hydrolases family 6 32-302 GH family 6 protein (P. halstedii) (XP_024583306.1) 81.82 1-20

Table 3

Secondary structure and tertiary structure of PvGH proteins"

蛋白
Protein		 二级结构 Secondary structure 三级结构 Tertiary structure
α-螺旋
α-helix (%)		 β-转角
β-turn (%)		 无规则卷曲Random coil (%) 延伸链
Extend (%)		 与之最相似的蛋白
<BOLD>M</BOLD>ost similar protein		 相似性
<BOLD>S</BOLD>imilarity (%)
PvG11117 32.98 5.59 48.67 12.77 Glycoside hydrolase family 6 26.24
PvG13516 36.45 6.40 41.63 15.52 β-1,3-glucanosyltr-ansferase 31.56
PvG10113 36.22 6.63 45.15 11.99 Cellobiohydrolase cel6A 24.49
PvG01792 43.70 3.86 39.07 13.37 β-1,3-glucanosyltr-ansferase 33.33
PvG09279 5.71 5.71 49.61 38.96 Endo-polygalacturonase 39.88
PvG02199 14.47 7.78 56.80 20.95 1,4-β-Cellulase 59.86
PvG13517 41.05 3.31 39.67 15.98 β-1,3-Glucosyltransf-erase 30.30
PvG13010 34.71 6.34 42.98 15.98 Chimeric cel6A 26.82

Fig. 2

Tertiary structure of PvGH proteins"

Fig. 3

Functional validation of predicted signal peptide of PvGHs"

Fig. 4

The inhibition of PCD by PvGH proteins in N. benthamiana"

Fig. 5

Expression analysis of PvGHs at different stages of infection"

Fig. 6

The PvGH proteins promote infection of P. nicotianae Significant differences at P<0.05 level"

[1]
DEREVNINA L, PETRE B, KELLNER R, DAGDAS Y F, SAROWAR M N, GIANNAKOPOULOU A, DE LA CONCEPCION J C, CHAPARRO-GARCIA A, PENNINGTON H G, VAN WEST P, KAMOUN S. Emerging oomycete threats to plants and animals. Philosophical Transaction of the Royal Society of London, Series B, Biological Sciences, 2016, 371(1709): 20150459.
[2]
DEREVNINA L, DAGDAS Y F, DE LA CONCEPCION J C, BIALAS A, KELLNER R, PETRE B, DOMAZAKIS E, DU J, WU C H, LIN X, AGUILERA-GALVEZ C, CRUZ-MIRELES N, VLEESHOUWERS V G, KAMOUN S. Nine things to know about elicitins. New Phytologist, 2016, 212(4): 888-895.

doi: 10.1111/nph.14137 pmid: 27582271
[3]
MCGOWAN J FITZPATRICK D A. Genomic, network, and phylogenetic analysis of the oomycete effector arsenal. mSphere, 2017, 2(6): e00408-17.
[4]
FEI H, FEIL W S, CHAIN P, LARIMER F, DI BARTOLO G, COPELAND A, LYKIDIS A, TRONG S, NOLAN M, GOLTSMAN E, et al. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(31): 11064-11069.
[5]
COUTINHO P M, ANDERSEN M R, KOLENOVA K, VAN KUYK P A, BENOIT I, GRUBEN B S, TREJO-AGUILAR B, VISSER H, VAN SOLINGEN P, PAKULA T, et al. Post-genomic insights into the plant polysaccharide degradation potential of Aspergillus nidulans and comparison to Aspergillus niger and Aspergillus oryzae. Fungal Genetics and Biology, 2009, 46(Suppl. 1): S161-S169.

doi: 10.1016/j.fgb.2008.07.020
[6]
BATTAGLIA E, BENOIT I, VAN DEN BRINK J, WIEBENGA A, COUTINHO P M, HENRISSAT B, DE VRIES R P. Carbohydrate- active enzymes from the Zygomycete fungus Rhizopus oryzae: A highly specialized approach to carbohydrate degradation depicted at genome level. BMC Genomics, 2011, 12: 38.

doi: 10.1186/1471-2164-12-38
[7]
VANFOSSEN A L, QZDEMIR I, ZELIN S L, KELLY R M. Glycoside hydrolase inventory drives plant polysaccharide deconstruction by the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus. Biotechnology and Bioengineering, 2011, 108(7): 1559-1569.

doi: 10.1002/bit.23093
[8]
WHITNEY J C, CHOU S, RUSSELL A B, BIBOY J, GARDINER T E, FERRIN M A, BRITTNACHER M, VOLLMER W, MOUGOUS J D. Identification, structure, and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. The Journal of Biological Chemistry, 2013, 288(37): 26616-26624.

doi: 10.1074/jbc.M113.488320
[9]
MA Z C, SONG T Q, ZHU L, YE W W, WANG Y, SHAO Y Y, DONG S M, ZHANG Z G, DOU D L, ZHENG X B, TYLER B M, WANG Y C. A Phytophthora sojae glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP. The Plant Cell, 2015, 27(7): 2057-2072.

doi: 10.1105/tpc.15.00390
[10]
ÖKMEN B, BACHMANN D, PIERRE J, DE WIT P J. A conserved GH17 glycosyl hydrolase from plant pathogenic Dothideomycetes releases a DAMP causing cell death in tomato. Molecular Plant Pathology, 2019, 20(12): 1710-1721.

doi: 10.1111/mpp.12872 pmid: 31603622
[11]
朱林. 大豆疫霉病原相关模式分子PsXEGl的免疫活性和毒性功能分析[D]. 南京: 南京农业大学, 2016.
ZHU L. Analysis of the immune activity and virulence function of the PAMP PsXEG1 secreted by Phytopphthora sojae[D]. Nanjing: Nanjing Agricultural University, 2016.(in Chinese)
[12]
MA Z C, ZHU L, SONG T Q, WANG Y, ZHANG Q, XIA Y Q, QIU M, LIN Y C, LI H Y, KONG L, et al. A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG 1 from a host inhibitor. Science, 2017, 355(6326): 710-714.

doi: 10.1126/science.aai7919
[13]
ZHU W J, RONEN M, GUR Y, MINZ-DUB A, MASRATI G, BEN-TAL N, SAVIDOR A, SHARON I, EIZNER E, VALERIUS O, BRAUS G H, BOWLER K, BAR-PELED M, SHARON A. BcXYG1, a secreted xyloglucanase from Botrytis cinerea, triggers both cell death and plant immune responses. Plant Physiology, 2017, 175: 438-456.

doi: 10.1104/pp.17.00375
[14]
YANG Y K, YANG X F, DONG Y J, QIU D W. The Botrytis cinerea xylanase BcXyl1 modulates plant immunity. Frontiers in Microbiology, 2018, 9: 2535.

doi: 10.3389/fmicb.2018.02535
[15]
GUI Y J, CHEN J Y, ZHANG D D, LI N Y, LI T G, ZHANG W Q, WANG X Y, SHORT D, LI L, KONG Z Q, BAO Y M, SUBBARAO K V, DAI X F. Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate- binding module 1. Environmental Microbiology, 2017, 19(5): 1914-1932.

doi: 10.1111/1462-2920.13695
[16]
GUI Y J, ZHANG W Q, ZHANG D D, ZHOU L, SHORT D P G, WANG J, MA X F, LI T G, KONG Z Q, WANG B L, WANG D, LI N Y, SUBBARAO K V, CHEN J Y, DAI X F. A Verticillium dahliae extracellular cutinase modulates plant immune responses. Molecular Plant-Microbe Interactions, 2018, 31(2): 260-273.

doi: 10.1094/MPMI-06-17-0136-R
[17]
YANG Y K, ZHANG Y, LI B B, YANG X F, DONG Y J, QIU D W. A Verticillium dahliae pectate lyase induces plant immune responses and contributes to virulence. Frontiers in Plant Science, 2018, 9: 1271.

doi: 10.3389/fpls.2018.01271
[18]
ZHANG L, YAN J P, FU Z C, SHI W J, NINKUU V, LI G Y, YANG X F, ZENG H M. FoEG1, a secreted glycoside hydrolase family 12 protein from Fusarium oxysporum, triggers cell death and modulates plant immunity. Molecular Plant Pathology, 2021, 22(5): 522-538.

doi: 10.1111/mpp.13041
[19]
ZHANG L, KARS I, ESSENSTAM B, LIEBRAND T W, WAGEMAKERS L, ELBERSE J, TAGKALAKI P, TJOITANG D, VAN DEN ACKERVEKEN G, VAN KAN J A. Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the Arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiology, 2014, 164(1): 352-364.

doi: 10.1104/pp.113.230698
[20]
RON M, AVNI A. The receptor for the fungal elicitor ethylene- inducing xylanase is a member of a resistance-like gene family in tomato. The Plant Cell, 2004, 16(6): 1604-1615.

doi: 10.1105/tpc.022475
[21]
YIN Z Y, WANG N, PI L, LI L, DUAN W W, WANG X D, DOU D L. Nicotiana benthamiana LRR-RLP NbEIX2 mediates the perception of an EIX-like protein from Verticillium dahliae. Journal of Integrative Plant Biology, 2021, 63(5): 949-960.

doi: 10.1111/jipb.v63.5
[22]
YIN L, AN Y, QU J J, LI X L, ZHANG Y L, DRY I, WU H, LU J. Genome sequence of Plasmopara viticola and insight into the pathogenic mechanism. Scientific Reports, 2017, 7: 46553.

doi: 10.1038/srep46553
[23]
尹玲. 葡萄霜霉病抗性基因MrRPV1结构域及霜霉菌效应分子功能研究[D]. 北京: 中国农业大学, 2015.
YIN L. Functional analysis of domains of grape downy mildew resistance gene MrRPV1 and effectors of Plasmopara viticola[D]. Beijing: China Agricultural University, 2015.(in Chinese)
[24]
刘云霄. 葡萄霜霉菌RXLR效应蛋白鉴定及其功能分析[D]. 北京: 中国农业大学, 2018.
LIU Y X. Characterization and functional analysis of grapevine downy mildew RXLR effectors[D]. Beijing: China Agricultural University, 2018.(in Chinese)
[25]
CHENG Y L, WU K, YAO J N, LI S M, WANG X J, HUANG L L, KANG Z S. PSTha5a23, a candidate effector from the obligate biotrophic pathogen Puccinia striiformis f. sp. tritici, is involved in plant defense suppression and rust pathogenicity. Environmental Microbiology, 2017, 19(5): 1717-1729.

doi: 10.1111/1462-2920.13610
[26]
黄振, 李慧雪, 周宇明, 暴怡雪, 张木清, 姚伟. 甘蔗梢腐病病原菌Fusarium sacchari Nep1-like蛋白的筛选鉴定及功能分析. 植物病理学报, 2022, 52(2): 156-164.
HUANG Z, LI H X, ZHOU Y M, BAO Y X, ZHANG M Q, YAO W. Identification and function analysis of Nep1-like proteins of Fusarium sacchari, the pathogen of sugarcane pokkah boeng disease. Acta Phytopathologica Sinica, 2022, 52(2): 156-164.(in Chinese)
[27]
VIDHYASEKARAN P. PAMP Signals in Plant Innate Immunity. Springer, 2014.
[28]
LACOMME C, SANTA CRUZ S. Bax-induced cell death in tobacco is similar to the hypersensitive response. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96(14): 7956-7961.
[29]
TAN X W, HU Y Y, JIA Y L, HOU X Y, XU Q, HAN C, WANG Q Q. A conserved glycoside hydrolase family 7 cellobiohydrolase PsGH7a of Phytophthora sojae is required for full virulence on soybean. Frontiers in Microbiology, 2020, 11: 1285.

doi: 10.3389/fmicb.2020.01285
[30]
贾玉丽. 大豆疫霉胞外纤维素降解酶PsGH7c的功能初探[D]. 泰安: 山东农业大学, 2021.
JIA Y L. Preliminary studies on the function of extracellular cellulase PsGH7c from Phytophthora sojae[D]. Taian: Shandong Agricultural University, 2021.(in Chinese)
[31]
CHEN J L, INOUE Y, KUMAKURA N, MISE K, SHIRASU K, TAKANO Y. Comparative transient expression analyses on two conserved effectors of Colletotrichum orbiculare reveal their distinct cell death-inducing activities between Nicotiana benthamiana and melon. Molecular Plant Pathology, 2021, 22(8): 1006-1013.

doi: 10.1111/mpp.13078
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