不同抗性柑橘对野生型和柑橘链格孢毒素合成受阻褐斑病菌侵染的转录响应差异

doi:10.3785/j.issn.1008-9209.2022.12.221

浙江大学学报（农业与生命科学版）

2023, Vol. 49

Issue (6): 787-801 DOI: 10.3785/j.issn.1008-9209.2022.12.221

植物保护

不同抗性柑橘对野生型和柑橘链格孢毒素合成受阻褐斑病菌侵染的转录响应差异

马慧¹(

),马海杰²,焦晨¹,李红叶¹(

)

^1.农业农村部作物病虫分子生物学重点实验室/浙江省作物病虫生物学重点实验室/浙江大学农业与生物技术学院, 浙江杭州 310058
^2.农业农村部亚热带果品蔬菜质量安全控制重点实验室/浙江农林大学园艺科学学院, 浙江杭州 311300

Differential transcriptome analysis of different resistant citrus varieties infected with wild-type and toxin synthesis-impaired strains causing Alternaria brown spot

Hui MA¹(

),Haijie MA²,Chen JIAO¹,Hongye LI¹(

)

^1.Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insects/Zhejiang Provincial Key Laboratory of Biology of Crop Pathogens and Insects/College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, Zhejiang, China
^2.Ministry of Agriculture and Rural Affairs Key Laboratory of Quality and Safety Control of Subtropical Fruits and Vegetables/College of Horticulture Science, Zhejiang A&F University, Hangzhou 311300, Zhejiang, China

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摘要：

为探讨不同抗性柑橘在与褐斑病菌互作过程中对柑橘链格孢毒素的响应差异，以抗病品种克里曼丁（Citrus clementina Hort. ex Tan. cv. Clementine）和感病品种丹西红橘（Citrus reticulata Blanco cv. Dancy）为材料，分别接种野生型产毒菌株Z7和毒素合成基因ACTT6双敲除突变体菌株ΔΔACTT6，并利用转录组测序技术对接种24 h和48 h后的叶片进行基因表达分析。比较2种柑橘对产毒和不产毒菌株侵染后的转录差异发现，2个品种的先天免疫通路（病原物相关分子模式触发的免疫反应和效应子触发的免疫反应）、病程相关蛋白、WRKY转录因子、次生代谢途径等基因均受产毒菌株诱导表达。在接种后期（48 h），产毒菌株主要激活感病品种的脂质和蛋白质等大分子降解过程，说明其细胞完整性因毒素产生而遭到破坏；而抗病柑橘则主要富集解毒和茉莉酸代谢等生物过程，其中特异激活的多药及毒素化合物外排蛋白（multidrug and toxic compound extrusion protein, MATE）基因与其抵御褐斑病菌毒素的能力有关。本研究初步明确了柑橘对褐斑病菌毒素响应的分子调控机制和关键功能基因，可为柑橘抗褐斑病菌分子育种提供理论依据。

关键词： 柑橘褐斑病; 链格孢菌橘致病型; 柑橘链格孢毒素; 转录组

Abstract:

To investigate the differences in the response of citrus varieties with different resistances to Alternaria citri toxin (ACT) during interaction with the Alternaria alternata pathotype tangerine causing Alternaria brown spot, we inoculated the wild-type toxin-producing strain Z7 and the ACT synthesis-impaired mutant strain ΔΔACTT6 onto the leaves of resistant variety Clementine (Citrus clementina Hort. ex Tan. cv. Clementine) and the susceptible variety Dancy (Citrus reticulata Blanco cv. Dancy), and analyzed the gene expressions at 24 h and 48 h after inoculation using transcriptome sequencing technology. By comparing the corresponding differences in transcription between the two citrus varieties against the toxin-producing and non-toxin-producing strains, we found that the genes involved in the pathogen-associated molecular patterns (PAMPs)-triggered immunity (PTI) and effector-triggered immunity (ETI) pathways, pathogenesis-related proteins, WRKY transcription factors, and the secondary metabolic pathway were induced by the toxin-producing strain in both the varieties. At the later stage of inoculation (48 h), the toxin-producing strain mainly activated macromolecular degradation processes such as lipid and protein degradation in the susceptible citrus variety, indicating that its cellular integrity was disrupted due to toxin production, whereas the resistant citrus variety was mainly enriched in biological processes such as detoxification and jasmonic acid metabolism. Some multidrug and toxic compound extrusion protein (MATE) genes were specifically activated in the resistant citrus variety, which implies their ability to resist fungal toxins. In conclusion, the molecular regulatory mechanisms and key functional genes involved in the response of citrus varieties to ACT are preliminarily clarified, which provide a theoretical basis for the molecular breeding of citruses against Alternaria brown spot.

Key words: Alternaria brown spot Alternaria alternata pathotype tangerine Alternaria citri toxin transcriptome

收稿日期: 2022-12-22 出版日期: 2023-12-25

CLC:

S432.1

基金资助: 国家现代农业（柑橘）产业技术体系建设专项(CARS-26);国家自然科学基金项目(32102148);浙江省重点研发计划项目(2019C02022)

通讯作者: 李红叶 E-mail: huim@zju.edu.cn;hyli@zju.edu.cn

作者简介: 马慧（https://orcid.org/0000-0002-0643-1763），E-mail：huim@zju.edu.cn

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引用本文:

马慧,马海杰,焦晨,李红叶. 不同抗性柑橘对野生型和柑橘链格孢毒素合成受阻褐斑病菌侵染的转录响应差异[J]. 浙江大学学报（农业与生命科学版）, 2023, 49(6): 787-801.

Hui MA,Haijie MA,Chen JIAO,Hongye LI. Differential transcriptome analysis of different resistant citrus varieties infected with wild-type and toxin synthesis-impaired strains causing Alternaria brown spot. Journal of Zhejiang University (Agriculture and Life Sciences), 2023, 49(6): 787-801.

链接本文:

https://www.zjujournals.com/agr/CN/10.3785/j.issn.1008-9209.2022.12.221 或 https://www.zjujournals.com/agr/CN/Y2023/V49/I6/787

基因名称

Gene name

基因标识符

Gene ID

引物序列（5 $′$ →3 $′$ ）

Primer sequence (5 $′$ →3 $′$ )

几丁质酶基因

Chitinase gene

Cs1g029150

F: TCCAGAACCAGAAAGCAGTCT

R: ACAACTACGGTCCAGCAGGA

通用型调节因子2基因

General regulatory factor 2 gene

Cs3g011250

F: AATTGGCTCCGACTCATCCC

R: GGCCAAATTGCAAGCACGAT

半乳糖基转移酶基因

Galactosyltransferase gene

Cs4g021530

F: CAAGCCAGGACAACATGACTT

R: AGCAGGATCAGAGAACAAGCA

果胶酯酶基因

Pectinesterase gene

Cs4g022700

F: ACCGTCCTTGTTAGTTCGAAT

R: GGCTCAAGATGGAACTGGCA

脂质转移蛋白基因

Lipid-transfer protein gene

Cs4g023990

F: GGTCGACTGGTGGCTTGATC

R: CCCGAAGCACAGGAAACCTA

类甜蛋白基因

Thaumatin-like protein gene

Cs5g040330

F: CTTCGGTCTTGAACACGGGA

R: CCGTGTGATTAGATGTACGGC

肌动蛋白基因（内参基因）

Actin gene (reference gene)

CsActin

F: CATCCCTCAGCACCTTCC

R: CCAACCTTAGCACTTCTCC

表1 用于qRT-PCR验证的基因及引物序列

图1 抗病柑橘克里曼丁和感病柑橘丹西红橘叶片接种后的症状表现A.接种毒素合成基因ACTT6双敲除突变体菌株ΔΔACTT6；B.接种柑橘褐斑病菌野生型菌株Z7。

图2 不同处理组间差异表达基因（DEGs）比较hpi：接种后时间；CM：克里曼丁；DC：丹西红橘；Ai：毒素合成基因ACTT6双敲除突变体菌株诱导；Wi：野生型菌株诱导（下同）。灰色圆点表示没有DEGs；黑色圆点表示独有的DEGs数目；黑色圆点之间的连线表示比较组间共有的DEGs数目。

图3 差异表达基因的GO富集

图4 不同防御反应中的差异表达基因热图PRs：病程相关蛋白；PRRs：模式识别受体；JA：茉莉酸；PAL：苯丙氨酸氨裂合酶；4CL：4-香豆酸-辅酶A连接酶；MATE：多药及毒素化合物外排蛋白；NLRs：核苷酸结合域和富含亮氨酸重复序列蛋白。

图5 差异表达基因的qRT-PCR验证A.野生型菌株诱导；B.毒素合成基因ACTT6双敲除突变体菌株诱导。FC：差异倍数。

通路标识符 Pathway ID	通路名称 Pathway name	注释基因数 Number of annotated genes	p值 p-value
通路标识符 Pathway ID	通路名称 Pathway name	注释基因数 Number of annotated genes	24hpiCM-Wi	24hpiCM-Ai	48hpiCM-Wi	48hpiCM-Ai	24hpiDC-Wi	24hpiDC-Ai	48hpiDC-Wi	48hpiDC-Ai
map01120	不同环境中的微生物代谢 Microbial metabolism in diverse environments	334	＞0.050	＞0.050	＞0.050	0.000	0.018	＞0.050	0.000	＞0.050
map04016	植物MAPK信号通路 MAPK signaling pathway—plant	132	0.017	＞0.050	＞0.050	＞0.050	0.004	＞0.050	0.044	＞0.050
map01230	氨基酸生物合成 Biosynthesis of amino acids	194	0.015	＞0.050	＞0.050	＞0.050	0.000	＞0.050	0.000	＞0.050
map00196	光合作用-天线蛋白 Photosynthesis-antenna proteins	17	＞0.050	＞0.050	＞0.050	0.000	＞0.050	0.020	＞0.050	0.001
map04075	植物激素信号转导 Plant hormone signal transduction	254	0.016	＞0.050	＞0.050	＞0.050	＞0.050	0.000	＞0.050	0.002
map01200	碳代谢 Carbon metabolism	246	＞0.050	＞0.050	＞0.050	0.000	＞0.050	＞0.050	0.000	＞0.050
map00480	谷胱甘肽代谢 Glutathione metabolism	117	＞0.050	＞0.050	＞0.050	＞0.050	0.022	＞0.050	0.013	＞0.050
map00400	苯丙氨酸-酪氨酸-色氨酸生物合成 Phenylalanine, tyrosine and tryptophan biosynthesis	44	＞0.050	＞0.050	＞0.050	＞0.050	0.000	＞0.050	0.005	＞0.050
map00966	硫代葡萄糖苷生物合成 Glucosinolate biosynthesis	19	＞0.050	＞0.050	＞0.050	＞0.050	0.019	＞0.050	0.029	＞0.050
map01210	2-氧代羧酸代谢 2-oxocarboxylic acid metabolism	59	＞0.050	＞0.050	＞0.050	＞0.050	0.022	＞0.050	0.002	＞0.050
map00980	细胞色素P450对外源性物质的代谢 Metabolism of xenobiotics by cytochrome P450	79	＞0.050	＞0.050	＞0.050	＞0.050	0.005	＞0.050	0.013	＞0.050
map00592	α-亚麻酸代谢 Alpha-linolenic acid metabolism	54	＞0.050	＞0.050	＞0.050	＞0.050	0.028	＞0.050	0.001	＞0.050
map00195	光合作用 Photosynthesis	48	＞0.050	＞0.050	＞0.050	0.000	＞0.050	＞0.050	＞0.050	0.000
map00640	丙酸盐代谢 Propanoate metabolism	42	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.018	＞0.050
map00330	精氨酸和脯氨酸代谢 Arginine and proline metabolism	51	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.044	＞0.050
map04136	其他自噬 Autophagy-other	32	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.001	＞0.050
map03050	蛋白酶体 Proteasome	43	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.000	＞0.050
map00410	β-丙氨酸代谢 Beta-alanine metabolism	39	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.021	＞0.050
map04024	环腺苷酸信号通路 cAMP signaling pathway	42	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.041	＞0.050
map00280	缬氨酸、亮氨酸和异亮氨酸降解 Valine, leucine and isoleucine degradation	51	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.044	＞0.050
map00010	糖酵解/糖异生 Glycolysis/gluconeogenesis	114	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.001	＞0.050
map00020	三羧酸循环 Tricarboxylic acid cycle	44	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.000	＞0.050
map00620	丙酮酸代谢 Pyruvate metabolism	97	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.044	＞0.050
map04070	磷脂酰肌醇信号系统 Phosphatidylinositol signaling system	55	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.044	＞0.050
map00071	脂肪酸降解 Fatty acid degradation	47	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.004	＞0.050
map04072	磷脂酶D信号通路 Phospholipase D signaling pathway	34	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	0.038	＞0.050
map00520	氨基糖和核苷酸糖代谢 Amino sugar and nucleotide sugar metabolism	108	＞0.050	＞0.050	0.049	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050
map00630	乙醛酸和二羧酸代谢 Glyoxylate and dicarboxylate metabolism	69	＞0.050	＞0.050	＞0.050	0.040	＞0.050	＞0.050	＞0.050	＞0.050
map00710	光合生物的固碳作用 Carbon fixation in photosynthetic organisms	65	＞0.050	＞0.050	＞0.050	0.000	＞0.050	＞0.050	＞0.050	＞0.050
map00460	氰基氨基酸代谢 Cyanoamino acid metabolism	50	＞0.050	＞0.050	＞0.050	＞0.050	0.050	＞0.050	＞0.050	＞0.050
map00940	苯丙素类化合物生物合成 Phenylpropanoid biosynthesis	142	＞0.050	＞0.050	＞0.050	＞0.050	0.004	＞0.050	＞0.050	＞0.050
map00905	油菜素甾醇类化合物生物合成 Brassinosteroid biosynthesis	23	0.013	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050	＞0.050

表2 差异表达基因的KEGG通路富集

图3 差异表达基因的GO富集BP：生物过程（Biological process）。

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