Changes in phytohormone levels and gene expression of potato plants in response to potato virus Y and a nonvector insect

doi:10.3785/j.issn.1008-9209.2022.03.301

Journal of Zhejiang University (Agriculture and Life Sciences)

2023, Vol. 49

Issue (2): 167-178 DOI: 10.3785/j.issn.1008-9209.2022.03.301

Special Topic: Insect Physiology and Biochemistry & Pest Biological Control

Changes in phytohormone levels and gene expression of potato plants in response to potato virus Y and a nonvector insect

Yang GE¹(

),Jian ZHONG¹,Yadong ZHANG¹,Xiaoli HE¹,Lining LIU²,Asim MUNAWAR¹,Lijuan MAO³,Zengrong ZHU¹,Yi XU^4,⁵,Wenwu ZHOU¹(

)

^1.Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University/Zhejiang Provincial Key Laboratory of Biology of Crop Pathogens and Insects/Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Hangzhou 310058, Zhejiang, China
^2.College of Plant Protection, China Agricultural University, Beijing 100193, China
^3.Analysis Center of Agrobiology and Environmental Sciences (ACAES), Zhejiang University, Hangzhou 310058, Zhejiang, China
^4.Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, Jiangsu, China
^5.Key Laboratory of Plant Immunity, Nanjing Agricultural University, Nanjing 210095, Jiangsu, China

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Abstract

Potato virusY (PVY) and its nonvector insect of potato tuber moth (Phthorimaea operculella) are important disease and pest in global potato industry. In order to investigate whether PVY infection changed the physiological responses of potato plant to P. operculella, we studied performances of P. operculella on PVY-infected and non-infected healthy plants, and carried out the phytohormone analysis and comparative transcriptomic analysis for potato leaves which were affected by PVY infection and herbiory stimuli (dealing with the oral secretions of potato tuber moth), or co-stressed treatment. The results showed that the resistance to P. operculella was significantly increased in potato plants infected by PVY. Moreover, PVY infection also inhibited the increase of abscisic acid induced by herbivory stimuli. Compared with the healthy control plants, herbivory stimuli and PVY infection treatments produced 3 998 and 104 differentially expressed genes (DEGs), respectively; while 9 178 DEGs were induced by co-stressed treatment, suggesting that the co-stressed treatment may greatly affected the physiological responses in potato plants. Compared with the herbivory stimuli, the co-stressed plants had 743 DEGs, and many of them belong to the transferase activity, the protein processing in endoplasmic reticulum, and the phenylpropanoid biosynthesis pathways. And the expression levels of many genes in abscisic acid synthesis pathway were also down-regulated, which was consisted with the change of this phytohormone. In summary, this study systematically analyzed the physiological responses of potato plant confronted by the single- and co-stressed treatments of PVY infection and herbivory stimuli, which may provide scientific basis for exploring plant-virus-nonvector insect interactions.

Key words： potato potato virus Y Phthorimaea operculella co-stressed treatment physiological response

Received: 30 March 2022 Published: 25 April 2023

CLC:

S435.32

Corresponding Authors: Wenwu ZHOU E-mail: 21916167@zju.edu.cn;wenwuzhou@zju.edu.cn

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	Yang GE
	Jian ZHONG
	Yadong ZHANG
	Xiaoli HE
	Lining LIU
	Asim MUNAWAR
	Lijuan MAO
	Zengrong ZHU
	Yi XU
	Wenwu ZHOU

Cite this article:

Yang GE,Jian ZHONG,Yadong ZHANG,Xiaoli HE,Lining LIU,Asim MUNAWAR,Lijuan MAO,Zengrong ZHU,Yi XU,Wenwu ZHOU. Changes in phytohormone levels and gene expression of potato plants in response to potato virus Y and a nonvector insect. Journal of Zhejiang University (Agriculture and Life Sciences), 2023, 49(2): 167-178.

URL:

https://www.zjujournals.com/agr/10.3785/j.issn.1008-9209.2022.03.301 OR https://www.zjujournals.com/agr/Y2023/V49/I2/167

马铃薯应对马铃薯Y病毒与非介体昆虫胁迫的植物激素水平和基因表达变化

马铃薯Y病毒（potato virus Y, PVY）及其非介体昆虫马铃薯块茎蛾（Phthorimaea operculella）是世界马铃薯产业的重要病虫害，为探究PVY是否影响马铃薯对马铃薯块茎蛾的生理响应，本研究分析了马铃薯块茎蛾在PVY侵染和健康对照植株上的生长表现，并对无病虫害、PVY侵染、模拟虫害处理（用马铃薯块茎蛾口腔分泌物涂抹），以及PVY侵染和模拟虫害协同处理的植株叶片进行了植物激素测定和比较转录组分析。结果显示：马铃薯感染PVY后对马铃薯块茎蛾的抗性显著提高；PVY侵染可抑制模拟虫害造成的脱落酸含量上升；与健康对照组相比，模拟虫害和PVY侵染处理分别诱导产生3 998个和104个差异表达基因，而两者协同处理可诱导产生9 178个差异表达基因，说明这2种胁迫共存对马铃薯产生了极大的生理影响。与模拟虫害处理相比，PVY侵染和模拟虫害协同处理诱导产生743个差异表达基因，而这些基因主要富集在转移酶活性、内质网中蛋白质加工、苯丙素生物合成等通路中，而脱落酸合成通路中众多基因表达下调，与该植物激素变化情况一致。综上所述，本研究系统分析了马铃薯应对PVY侵染、马铃薯块茎蛾模拟虫害以及两者协同处理的生理反应，为探究“植物-病毒-非介体昆虫”三者互作提供了科学依据。

关键词： 马铃薯, 马铃薯Y病毒, 马铃薯块茎蛾, 协同处理, 生理响应

Table 1 Phytohormone pathway genes

序号 No.	基因编号 Gene ID	基因名称 Gene name	引物序列（5 $′$ →3 $′$ ） Primer sequence (5 $′$ →3 $′$ )
1	1494052	马铃薯Y病毒包被蛋白 PVY coat protein	F: AACCTCGCCAAATGTCAACG
1	1494052	马铃薯Y病毒包被蛋白 PVY coat protein	R: TTGCCTAAGGGTTGGTTTTGC
2	102606100	真核翻译起始因子3亚基E Eukaryotic translation initiation factor 3 subunit E	F: GGAGCACAGGAGAAGATGAAGGAG
2	102606100		R: CGTTGGTGAATGCGGCAGTAGG
3	PGSC0003DMG402001531	内切几丁质酶样蛋白 Endochitinase-like protein	F: ATCGCTGCATTTTTGGCTCA
3	PGSC0003DMG402001531	内切几丁质酶样蛋白 Endochitinase-like protein	R: GGGCTACCTCGTTCTTGCTT
4	PGSC0003DMG400030006	PAR-1b蛋白 PAR-1b protein	F: GACGGAGCGGTGAACAAGTA
4	PGSC0003DMG400030006	PAR-1b蛋白 PAR-1b protein	R: AGGGTATTCCGATTGACGCC
5	PGSC0003DMG400010859	脂肪氧合酶 Lipoxygenase	F: AGGATCTGCTGAGTACCCGT
5	PGSC0003DMG400010859	脂肪氧合酶 Lipoxygenase	R: TGTCCAAAACGCTCGTCTCT
6	PGSC0003DMG400008308	DNA复制许可因子MCM3同源物2 DNA replication licensing factor MCM3 homolog 2	F: ACCACCTTAGCTAGCCCGAT
6	PGSC0003DMG400008308		R:ATGGTCTTTTTCCCGCCCTT
7	PGSC0003DMG400005390	钙调素结合蛋白 Calmodulin-binding protein	F: ATGATGTGTGGCGTCTTGAA
7	PGSC0003DMG400005390	钙调素结合蛋白 Calmodulin-binding protein	R: CCGACATTCCATTTCCAAGT
8	PGSC0003DMG400002943	微粒体Ω-6-去饱和酶 Microsomal Ω-6-desaturase	F: AATGTGGTCACCATGGCTTT
8	PGSC0003DMG400002943	微粒体Ω-6-去饱和酶 Microsomal Ω-6-desaturase	R: TTGGAATGATGACGACGATG
9	PGSC0003DMG400033902	GATA-N结构域包含蛋白 GATA-N domain-containing protein	F: ATGTGGAGGAGGGATGGGTA
9	PGSC0003DMG400033902	GATA-N结构域包含蛋白 GATA-N domain-containing protein	R: ACGTGCGCATATCTTCCCAA
10	PGSC0003DMG400024310	富含甘氨酸RNA结合蛋白-1c RNA-binding glycine-rich protein-1c	F: GAAGGAAGATTGGTGGGACA
10	PGSC0003DMG400024310	富含甘氨酸RNA结合蛋白-1c RNA-binding glycine-rich protein-1c	R: CTTGCCTTGCTTCTCCACTC

Table 2 Primers used in qRT-PCR

Fig. 1 Potato inoculation phenotype and bioassay results of P. operculellaQuadruple asterisks (****) indicate extremely high significant differences at the 0.000 1 probability level.

Fig. 2 Dynamics of phytohormone levels in potato leavesThe concentrations of phytohormones are calculated by fresh mass. Single asterisk (*), double asterisks (**), triple asterisks (***), and quadruple asterisks (****) indicate significant differences at the 0.05, 0.01, 0.001, and 0.000 1 probability levels, respectively; n=5.

Table 3 Statistics of transcriptomic data output quality

Fig. 3 Venn diagram of DEGs numbers in different treatment groups compared with healthy control group

Fig. 4 Expression levels of genes in phytohormone pathways of co-stressed treatment (1 h) group compared with herbivory stimuli (1 h) groupFC: Fold change.

Fig. 5 Validation of transcriptomic sequencing data by qRT-PCRNumbers of 1-8 correspond to the genes represented by numbers of 3-10 in Table 2, respectively. FC: Fold change.


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