Scientia Agricultura Sinica ›› 2019, Vol. 52 ›› Issue (21): 3806-3818.doi: 10.3864/j.issn.0578-1752.2019.21.009

• PLANT PROTECTION • Previous Articles     Next Articles

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

ZOU XiuPing,LONG JunHong,PENG AiHong,CHEN Min,LONG Qin,CHEN ShanChun   

  1. National Center for Citrus Variety Improvement, Citrus Research Institute, Southwest University/Chinese Academy of Agricultural Sciences, Chongqing 400712
  • Received:2019-05-23 Accepted:2019-07-15 Online:2019-11-01 Published:2019-11-12

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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

Fig. 1

Resistance evaluation of CsGH3.6 transgenic plants to citrus bacterial canker"

Fig. 2

Analysis of free IAA content in CsGH3.6 transgenic plants Control：溃疡病菌侵染前自由IAA含量检测Free IAA content detection before Xcc inoculation;Xcc：溃疡病菌侵染3 d时自由IAA含量检测Free IAA content detection at 3 d after Xcc inoculation"

Fig. 3

Analysis of SA and JA contents in CsGH3.6 transgenic plants * represents significant difference compared with WT (Tukey’s test, P<0.05). The same as Fig. 4, Fig. 6"

Fig. 4

Phenotypes of CsGH3.6 transgenic plants"

Fig. 5

Microscopic observation of epidemic cells of CsGH3.6 transgenic plants"

Fig. 6

Statistical analysis of epidermal cell length (A) and stomatal density (B) of CsGH3.6 transgenic plants"

Fig. 7

Transcriptome sequencing analysis"

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

Fig. 8

Statistical analysis of differentially expressed genes related to biological stress"

Fig. 9

Statistical analysis of differentially expressed genes related to growth and development"

Table 2

Differentially expressed genes related to cell wall 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
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
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