超量表达CsGH3.6通过抑制生长素信号转导 增强柑橘溃疡病抗性

doi:10.3864/j.issn.0578-1752.2019.21.009

Abstract

Abstract:

【Background】 Citrus canker, induced by Xanthomonas citri subsp. citri (Xcc), is one of the most destructive disease in citrus production. Auxin plays an important role in regulating Xcc-induced pustule formation in citrus. GH3, an early auxin response gene, regulates plant hormone homeostasis through acylating indole-3-acetic acid (IAA). The previous study found that CsGH3.6 had a vital role in response to Xcc infection. 【Objective】 Here, to explore the internal mechanism of CsGH3.6 in regulating the dynamic balance of auxin and affecting the plant resistance to citrus canker, disease resistance evaluation, phenotype analysis, hormone determination and transcriptome sequencing of Wanjingcheng orange (Citrus sinensis) overexpressing CsGH3.6 were performed in this study.【Method】 To evaluate resistance to citrus canker in transgenic plants overexpressing CsGH3.6, fully expanded intact leaves gathered from transgenic plants were infected with Xcc by the pin-prick inoculation, and the diseased areas and disease severity index were investigated 10 d after inoculation, the wild type (WT) plant was used as the control. To detect hormone levels in transgenic plants, different hormones were isolated from leaves before and after Xcc infection and their contents were determined through high performance liquid chromatography (HPLC). Compared with WT plant, changes of phenotypes (plant types and leaf longitudinal diameter, transverse diameter and thickness) in transgenic plants were investigated in the greenhouse, and the length of epidermal cell and stomata density were further analyzed using optical microscopy. RNA sequencing was performed to investigate transcript changes in transgenic plant, and gene functions were annotated based on Nr, Nt, Pfam, COG, SwissProt and gene ontology (GO) databases. To elucidate the molecular mechanism of CsGH3.6 in regulating the canker resistance in citrus, the important genes, functions and pathways affected significantly by overexpressing CsGH3.6 were investigated using the KEGG database and MapMan software.【Result】 Overexpression of CsGH3.6 significantly enhanced citrus canker resistance in transgenic plants. The branches of transgenic plants increased and drooped, the leaves curled upward, became smaller and lighter in color. The stomata density of transgenic plants increased and the length of epidermal cells became shorter. Hormone analyses showed that the contents of free auxin IAA and jasmonic acid (JA) in transgenic plants decreased significantly, while the content of salicylic acid (SA) increased significantly. Transcriptome sequencing showed that overexpression of CsGH3.6 significantly inhibited the expression of auxin signal transduction related genes, especially the expression level of all the predicted Aux/IAA genes was down-regulated in transgenic plant. Conversely, the expression level of genes related to biological stress was up-regulated, most of which were pathogenesis-related genes. 【Conclusion】 Overexpression of CsGH3.6 can inhibit auxin signal transduction through acylating free IAA, regulate the homeostasis of JA and SA, change the morphogenesis of cells and plants, and finally enhance the plant resistance to citrus canker. The results suggest that the regulation of hormone homeostasis has potential value in citrus disease resistance breeding.

Key words: Xanthomonas citri subsp. citri (Xcc), citrus canker, auxin, CsGH3.6, resistance

ZOU XiuPing,LONG JunHong,PENG AiHong,CHEN Min,LONG Qin,CHEN ShanChun. Overexpression of CsGH3.6 Enhanced Resistance to Citrus Canker Disease by Inhibiting Auxin Signaling Transduction[J].Scientia Agricultura Sinica, 2019, 52(21): 3806-3818.

0
/ / Recommend

Add to citation manager EndNote|Reference Manager|ProCite|BibTeX|RefWorks

URL: https://www.chinaagrisci.com/EN/10.3864/j.issn.0578-1752.2019.21.009

https://www.chinaagrisci.com/EN/Y2019/V52/I21/3806

Figures/Tables 11

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Fig. 5

Fig. 6

Fig. 7

Table 1

Statistical analysis of differentially expressed genes related to auxin in the b19 transgenic plant"

基因编号Gene ID	推测的功能Putative function	差异倍数Log₂ fold change*
生长素合成-降解Auxin synthesis-degradation
Cs7g08110	IAA β-葡萄糖基转移酶 IAA β-glucosyltransferase	1.832
Orange1.1t02388	IAA β-D-葡萄糖基转移酶 IAA β-D-glucosyltransferase	-1.153
Cs3g19760	IAA氨基酸共轭水解酶 IAA amino acid conjugate hydrolase	1.573
Cs7g08080	IAA氨基酸共轭水解酶 IAA amino acid conjugate hydrolase	1.074
生长素运输Auxin transport
Orange1.1t00089	生长素输出载体PIN1 Auxin efflux carrier PIN1	-1.022
Cs2g16620	生长素输出载体PIN3 Auxin efflux carrier PIN3	-2.790
Cs3g19250	生长素运输相似蛋白3 Auxin transporter-like protein 3	-1.385
生长素信号转导Auxin signal transduction
Cs5g29060	AUX/IAA家族基因IAA11 AUX/IAA family IAA11	-1.570
Cs9g09120	AUX/IAA家族基因IAA13 AUX/IAA family IAA13	-1.286
Cs5g30380	AUX/IAA家族基因IAA16 AUX/IAA family IAA16	-3.052
Cs5g30390	AUX/IAA家族基因IAA4 AUX/IAA family IAA4	-3.905
Cs7g05540	AUX/IAA家族基因IAA29 AUX/IAA family IAA29	-3.067
Cs9g08100	AUX/IAA家族基因IAA29 AUX/IAA family IAA29	-4.314
Cs9g08110	AUX/IAA家族基因IAA4 AUX/IAA family IAA14	-5.958
Cs1g13970	AUX/IAA家族基因IAA22 AUX/IAA family AUX22	-6.028
Cs4g18240	AUX/IAA家族基因IAA29 AUX/IAA family IAA29	-3.097
cs1g13960	AUX/IAA家族基因 AUX/IAA family	-1.775
cs3g10920	AUX/IAA家族基因IAA22 AUX/IAA family IAA22	-1.656
cs3g10930	AUX/IAA家族基因IAA16 AUX/IAA family IAA16	-1.831
cs3g16750	AUX/IAA家族基因IAA9 AUX/IAA family IAA9	-1.089
Orange1.1t04221	SAUR-like相似蛋白ARG7 SAUR-like protein ARG7	-4.445
Cs8g16440	生长素响应因子ARF10 Auxin response factor ARF10	-1.931
cs4g04520	生长素响应因子ARF7 Auxin response factor ARF7	-1.111
cs4g12720	SAUR-like相似蛋白 SAUR-like protein	3.141
orange1.1t00825	IAA酰基化酶GH3.5 IAA-amido synthetase GH3.5	-1.200
cs4g11890	IAA酰基化酶CsGH3.6 IAA-amido synthetase CsGH3.6	7.325

Table 1

Fig. 8

Fig. 9

Table 2

References 42

[1]	何秀玲, 袁红旭 . 柑橘溃疡病发生与抗性研究进展. 中国农学通报, 2007,23(8):409-412.
	HE X L, YUAN H X . Research advances on the occurrence and resistance of citrus bacterial canker disease. Chinese Agricultural Science Bulletin, 2007,23(8):409-412. (in Chinese)
[2]	GONG X Q, LIU J H . Genetic transformation and genes for resistance to abiotic and biotic stresses in Citrus and its related genera.Plant Cell, Tissue and Organ Culture, 2013,113(2):137-147.
[3]	COSTACURTA A, MAZZAFERA P, ROSATO Y B . Indole-3-acetic acid biosynthesis by Xanthomonas axonopodis pv. citri is increased in the presence of plant leaf extracts. FEMS Microbiology Letters, 1998,159(2):215-220.
[4]	CERNADAS R A, CAMILLO L R, BENEDETTI C E . Transcriptional analysis of the sweet orange interaction with the citrus canker pathogensXanthomonas axonopodis pv. citri and Xanthomonas axonopodis pv.aurantifolii. Molecular Plant Pathology, 2008,9(5):609-631.
[5]	CERNADAS R A, BENEDETTI C E . Role of auxin and gibberellin in citrus canker development and in the transcriptional control of cell-wall remodeling genes modulated by Xanthomonas axonopodis pv. citri. Plant Science, 2009,177(3):190-195.
[6]	CHEN M, HE Y R, XU L Z, PENG A H, LEI T G, YAO L X, LI Q, ZHOU P F, BAI X J, DUAN M J, JIANG X Y, JIA R R, ZOU X P, CHEN S C . Cloning and expression analysis of Citrus genes CsGH3.1 and CsGH3.6 responding to Xanthomonas axonopodis pv. citri infection. Horticultural Plant Journal, 2016,2(4):193-202.
[7]	DUCA D, LORV J, PATTEN C L, ROSE D, GLICK B R . Indole-3- acetic acid in plant-microbe interactions. Antonie Van Leeuwenhoek, 2014,106(1):85-125.
[8]	傅晶 . 抑制病原菌诱导的生长素的积累赋予水稻广谱抗性[D]. 武汉: 华中农业大学, 2010.
	FU J . Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice[D]. Wuhan: Huazhong Agricultural University, 2010. ( in Chinese)
[9]	FU J, LIU H B, LI Y, YU H H, LI X H, XIAO J H, WANG S P . Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice. Plant Physiology, 2011,155(1):589-602.
[10]	MUTKA A M, FAWLEY S, TSAO T, KUNKEL B N . Auxin promotes susceptibility to Pseudomonas syringae via a mechanism independent of suppression of salicylic acid-mediated defenses.The Plant Journal, 2013,74(5):746-754.
[11]	ROBERT-SEILANIANTZ A, GRANT M ,JONES J D G. Hormone crosstalk in plant disease and defense: More than just jasmonate-salicylate antagonism. Annual Review of Phytopathology, 2011,49:317-343.
[12]	CHEN Y, SHEN H, WANG M, LI Q, HE Z . Salicyloyl-aspartate synthesized by the acetyl-amido synthetase GH3.5 is a potential activator of plant immunity in Arabidopsis. Acta Biochimica et Biophysica Sinica, 2013,45(10):827-836.
[13]	WESTFALL C S, HERRMANN J, CHEN Q, WANG S, JEZ J M . Modulating plant hormones by enzyme action: The GH3 family of acyl acid amido synthetases.Plant Signaling & Behavior, 2010,5(12):1607-1612.
[14]	HAGEN G, GUILFOYLE T J . Rapid induction of selective transcription by auxins.Molecular and Cellular Biology, 1985,5(6):1197-1203.
[15]	DU H, WU N, FU J, WANG S P, LI X H, XIAO J H, XIONG L Z . A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice.Journal of Experimental Botany, 2012,63(18):6467-6480. doi: 10.1093/jxb/ers300
[16]	DOMINGO C, ANDRES F, THARREAU D, IGLESIAS D J, TALON M . Constitutive expression of OsGH3.1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice.Molecular Plant-Microbe Interactions, 2009,22(2):201-210.
[17]	DING X, CAO Y, HUANG L, ZHAO J, XU C, LI X, WANG S . Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice.The Plant Cell, 2008,20(1):228-240.
[18]	SINGH V K, JAIN M, GARG R. Genome-wide analysis and expression profiling suggest diverse roles of GH3 genes during development and abiotic stress responses in legumes.Frontiers in Plant Science, 2015,5: Article 789.
[19]	YUAN H, ZHAO K, LEI H, SHEN X, LIU Y, LIAO X, LI T . Genome-wide analysis of the GH3 family in apple (Malus × domestica).BMC Genomics, 2013,14:297.
[20]	FENG S, YUE R, TAO S, YANG Y, ZHANG L, XU M, WANG H, SHEN C . Genome-wide identification, expression analysis of auxin- responsive GH3 family genes in maize (Zea mays L.) under abiotic stresses.Journal of Integrative Plant Biology, 2015,57(9):783-795.
[21]	KUMAR R, AGARWAL P, TYAGI A K, SHARMA A K . Genome- wide investigation and expression analysis suggest diverse roles of auxin-responsive GH3 genes during development and response to different stimuli in tomato(Solanum lycopersicum).Molecular Genetics and Genomics, 2012,287(3):221-235.
[22]	YU D, QANMBER G, LU L, WANG L, LI J, YANG Z, LIU Z, LI Y, CHEN Q, MENDU V, LI F, YANG Z . Genome-wide analysis of cotton GH3 subfamily II reveals functional divergence in fiber development, hormone response and plant architecture.BMC Plant Biology, 2018,18:350.
[23]	YANG Y, YUE R, SUN T, ZHANG L, CHEN W, ZENG H, WANG H, SHEN C . Genome-wide identification, expression analysis of GH3 family genes in Medicago truncatula under stress-related hormones and Sinorhizobium meliloti infection.Applied Microbiology and Biotechnology, 2015,99(2):841-854.
[24]	陈敏 . 超量表达生长素早期响应基因CsGH3增强柑橘溃疡病抗性[D]. 重庆: 西南大学, 2017.
	CHEN M . Overexpressing early auxin-responsive gene CsGH3 enhances canker resistance in citrus[D]. Chongqing: Southwest University, 2017. ( in Chinese)
[25]	MARQUES J P R, AMORIM L, SILVA-JUNIOR G J, SPOSITO M B, APPEZZATO-DA GLÓRIA B.Structural and biochemical characteristics of citrus flowers associated with defence against a fungal pathogen. AoB Plants, 2014,7: plu090.
[26]	PENG A H, CHEN S C, LEI T G, XU L Z, HE Y R, WU L, YAO L X, ZOU X P . Engineering canker-resistant plants through CRISPR/Cas9- targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnology Journal, 2017,15:1509-1519.
[27]	THIMM O, BLASING O, GIBON Y, NAGEL A, MEYER S, KRUGER P, SELBIG J, MULLER L A, RHEE S Y, STITT M . MAPMAN: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.The Plant Journal, 2004,37(6):914-939.
[28]	GUTIERREZ L, MONGELARD G, FLOKOVÁ K ,PĂCURAR D I,NOVÁK O,STASWICK P,KOWALCZYK M,PĂCURAR M,DEMAILLY H,GEISS G,BELLINI C. Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. The Plant Cell, 2012,24(6):2515-2527.
[29]	HU Y, ZHANG J L, JIA H G, SOSSO D, LI T, FROMMER W B, YANG B, WHITE F F, WANG N, JONES J B . Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proceedings of the National Academy of Sciences of the United States of America, 2014,111(4):E521-E529.
[30]	BRUNINGS A M, GABRIEL D W . Xanthomonas citri: breaking the surface. Molecular Plant Pathology, 2003,4(3):141-157.
[31]	陈亮, 侯岁稳 . 植物气孔发育的分子遗传调控. 中国科学: 生命科学, 2017,47(8):798-807.
	CHEN L, HOU S W . Molecular genetic control of plant stomatal development. Scientia Sinica Vitae, 2017,47(8):798-807. (in Chinese)
[32]	周丽娟, 陈尔娟, 韩笑, 何用娟, 陈善娜, 陈小兰 . 激素与气孔发育研究进展. 西北植物学报, 2015,35(4):845-851.
	ZHOU L J, CHEN E J, HAN X, HE Y J, CHEN S N, CHEN X L . Review on hormone regulation of stomatal development. Acta Botanica Boreali-Occidentalia Sinica, 2015,35(4):845-851. (in Chinese)
[33]	LE J, LIU X G, YANG K Z, CHEN X L, ZOU J J, WANG H Z, WANG M, VANNESTE S, MORITA M, TASAKA M, DING Z J, FRIML J, BEECKMAN T, SACK F . Auxin transport and activity regulate stomatal patterning and development . Nature Communications, 2014,5:3090.
[34]	李敏, 段硕, 李中安, 周彦, 周常勇, 谭锦, 彭耀武 . 叶片微形态结构特征与柑桔溃疡病抗性的关系. 中国南方果树, 2013,42(2):1-5.
	LI M, DUAN S, LI Z A, ZHOU Y, ZHOU C Y, TAN J, PENG Y W . Analysis of relationship between citrus canker resistance and leaf micro-morphological characteristics. South China Fruits, 2013,42(2):1-5. (in Chinese)
[35]	温寿星, 黄镜浩, 陈瑾, 蔡子坚, 包榕, 张凌媛 . 叶片结构与柑橘溃疡病抗性的初步研究. 中国农学通报, 2009,25(13):66-69.
	WEN S X, HUANG J H, CHEN J, CAI Z J, BAO R, ZHANG L Y . Preliminary studies on leaves structure in resistant and susceptible cultivars of citrus. Chinese Agricultural Science Bulletin, 2009,25(13):66-69. (in Chinese)
[36]	FRANCIS M I, REDONDO A, BURNS J K, GRAHAM J H . Soil application of imidacloprid and related SAR-inducing compounds produces effective and persistent control of citrus canker.European Journal of Plant Pathology, 2009,124(2):283-292. doi: 10.1007/s10658-008-9415-x
[37]	ZHANG X, FRANCIS M I, DAWSON W O, GRAHAM J H, ORBOVIĆ V, TRIPLETT E W, MOU Z . Over-expression of the Arabidopsis NPR1 gene in citrus increases resistance to citrus canker.European Journal of Plant Pathology, 2010,128(1):91-100.
[38]	LI J, BRADER G, PALVA E T . The WRKY70 transcription factor: A node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense.The Plant Cell, 2004,16(2):319-331.
[39]	ZHANG Z, LI Q, LI Z, STASWICK P E, WANG M, ZHU Y, HE Z . Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction.Plant Physiology, 2007,145(2):450-464.
[40]	ZHAO Y . Auxin biosynthesis and its role in plant development.Annual Review of Plant Biology, 2010,61:49-64.
[41]	TIWARI S B, WANG X J, HAGEN G, GUILFOYLE T J . AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin.The Plant Cell, 2001,13(12):2809-2822.
[42]	宋二玲 . 三个病原物诱导启动子在转基因柑橘中受溃疡病菌和创伤诱导的表达分析[D]. 重庆: 西南大学, 2013.
	SONG E L . Canker bacterium- and wound-response characteristics of three pathogen-induced promoters in transgenic citrus[D]. Chongqing: Southwest University, 2013. ( in Chinese)

Metrics

Viewed

Full text

Abstract

Cited

Shared

Discussed

Comments

Recommended 0

No Suggested Reading articles found!

基因编号Gene ID	推测的功能Putative function	差异倍数Log₂ fold change
纤维素合成Cellulose synthesis
Cs4g02000	木质素特异纤维素合酶 Xylem-specific cellulose synthase	7.304
细胞壁蛋白Cell wall protein
Cs8g16830	成束蛋白样阿拉伯半乳聚糖蛋白12 FASCICLIN-like arabinogalactan-protein 12 FLA12	5.439
细胞壁修饰Cell wall modification
Cs4g03060	木葡聚糖内糖基转移酶相关蛋白 Xyloglucan endotransglycosylase-related protein (XTR6)	2.591
Cs4g03130		2.031
Cs4g03140		2.227
Cs5g28330	角质素合成酶相关基因LCAC Cutin synthesis-related gene LCAC	1.576
Orange1.1t00556	植物蜡质合成相关基因KCS1 Wax biosynthesis-related gene KCS1	1.408
Cs5g07854	延展蛋白EXLB1 Expansin EXLB1	-1.393

Overexpression of CsGH3.6 Enhanced Resistance to Citrus Canker Disease by Inhibiting Auxin Signaling Transduction

RichHTML

PDF

Abstract

Cite this article

share this article

Figures/Tables 11

References 42

Related Articles 15

Metrics

Comments

Recommended 0

[1]	ZHANG XiaoLi, TAO Wei, GAO GuoQing, CHEN Lei, GUO Hui, ZHANG Hua, TANG MaoYan, LIANG TianFeng. Effects of Direct Seeding Cultivation Method on Growth Stage, Lodging Resistance and Yield Benefit of Double-Cropping Early Rice [J]. Scientia Agricultura Sinica, 2023, 56(2): 249-263.
[2]	LIU Jiao,LIU Chang,CHEN Jin,WANG MianZhi,XIONG WenGuang,ZENG ZhenLing. Distribution Characteristics of Prophage in Multidrug Resistant Escherichia coli as well as Its Induction and Isolation [J]. Scientia Agricultura Sinica, 2022, 55(7): 1469-1478.
[3]	GUO ZeXi,SUN DaYun,QU JunJie,PAN FengYing,LIU LuLu,YIN Ling. The Role of Chalcone Synthase Gene in Grape Resistance to Gray Mold and Downy Mildew [J]. Scientia Agricultura Sinica, 2022, 55(6): 1139-1148.
[4]	YAN LeLe,BU LuLu,NIU Liang,ZENG WenFang,LU ZhenHua,CUI GuoChao,MIAO YuLe,PAN Lei,WANG ZhiQiang. Widely Targeted Metabolomics Analysis of the Effects of Myzus persicae Feeding on Prunus persica Secondary Metabolites [J]. Scientia Agricultura Sinica, 2022, 55(6): 1149-1158.
[5]	WANG Kai,ZHANG HaiLiang,DONG YiXin,CHEN ShaoKan,GUO Gang,LIU Lin,WANG YaChun. Definition and Genetic Parameters Estimation for Health Traits by Using on-Farm Management Data in Dairy Cattle [J]. Scientia Agricultura Sinica, 2022, 55(6): 1227-1240.
[6]	ZHANG YaLing, GAO Qing, ZHAO Yuhan, LIU Rui, FU Zhongju, LI Xue, SUN Yujia, JIN XueHui. Evaluation of Rice Blast Resistance and Genetic Structure Analysis of Rice Germplasm in Heilongjiang Province [J]. Scientia Agricultura Sinica, 2022, 55(4): 625-640.
[7]	WANG MengRui, LIU ShuMei, HOU LiXia, WANG ShiHui, LÜ HongJun, SU XiaoMei. Development of Artificial Inoculation Methodology for Evaluation of Resistance to Fusarium Crown and Root Rot and Screening of Resistance Sources in Tomato [J]. Scientia Agricultura Sinica, 2022, 55(4): 707-718.
[8]	XIANG MiaoLian, WU Fan, LI ShuCheng, WANG YinBao, XIAO LiuHua, PENG WenWen, CHEN JinYin, CHEN Ming. Effects of Melatonin Treatment on Resistance to Black Spot and Postharvest Storage Quality of Pear Fruit [J]. Scientia Agricultura Sinica, 2022, 55(4): 785-795.
[9]	HU ChaoYue, WANG FengTao, LANG XiaoWei, FENG Jing, LI JunKai, LIN RuiMing, YAO XiaoBo. Resistance Analyses on Wheat Stripe Rust Resistance Genes to the Predominant Races of Puccinia striiformis f. sp. tritici in China [J]. Scientia Agricultura Sinica, 2022, 55(3): 491-502.
[10]	TANG ZiYun,HU JianXin,CHEN Jin,LU YiXing,KONG LingLi,DIAO Lu,ZHANG FaFu,XIONG WenGuang,ZENG ZhenLing. Relationship Between Biofilm Formation and Molecular Typing of Staphylococcus aureus from Animal Origin [J]. Scientia Agricultura Sinica, 2022, 55(3): 602-612.
[11]	LI ZhiLing,LI XiangJu,CUI HaiLan,YU HaiYan,CHEN JingChao. Development and Application of ELISA Kit for Detection of EPSPS in Eleusine indica [J]. Scientia Agricultura Sinica, 2022, 55(24): 4851-4862.
[12]	ZHANG Qi,DUAN Yu,SU Yue,JIANG QiQi,WANG ChunQing,BIN Yu,SONG Zhen. Construction and Application of Expression Vector Based on Citrus Leaf Blotch Virus [J]. Scientia Agricultura Sinica, 2022, 55(22): 4398-4407.
[13]	DU JinXia,LI YiSha,LI MeiLin,CHEN WenHan,ZHANG MuQing. Evaluation of Resistance to Leaf Scald Disease in Different Sugarcane Genotypes [J]. Scientia Agricultura Sinica, 2022, 55(21): 4118-4130.
[14]	FENG AiQing,WANG CongYing,ZHANG MeiYing,CHEN Bing,FENG JinQi,CHEN KaiLing,WANG WenJuan,YANG JianYuan,SU Jing,ZENG LieXian,CHEN Shen,ZHU XiaoYuan. Pathotype Analysis of Xanthomonas oryzae pv. oryzae in Main Rice Producing Regions of China and Establishment of Differential Hosts of Near-Isogenic Lines [J]. Scientia Agricultura Sinica, 2022, 55(21): 4175-4195.
[15]	YAN Qiang,XUE Dong,HU YaQun,ZHOU YanYan,WEI YaWen,YUAN XingXing,CHEN Xin. Identification of the Root-Specific Soybean GmPR1-9 Promoter and Application in Phytophthora Root-Rot Resistance [J]. Scientia Agricultura Sinica, 2022, 55(20): 3885-3896.