小麦籽粒次生物质对麦红吸浆虫幼虫解毒酶活性及基因表达的影响

doi:10.3864/j.issn.0578-1752.2020.20.009

摘要/Abstract

摘要：

【目的】明确小麦灌浆期籽粒次生物质含量与麦红吸浆虫（Sitodiplosis mosellena）幼虫谷胱甘肽转移酶（glutathione S-transferase,GST）、羧酸酯酶（carboxylesterase,CarE）和细胞色素P450 酶系（cytochrome P450,CYP450）活性及相关基因表达的关系,探讨次生物质在小麦对麦红吸浆虫抗性中的作用及麦红吸浆虫的解毒代谢机制。【方法】2016年5月采用剥穗调查法对陕西省周至县试验田种植的4个抗虫和4个感虫小麦品种（系）进行麦红吸浆虫幼虫危害调查,并收集各品种（系）灌浆期籽粒及取食各品种（系）灌浆期籽粒的麦红吸浆虫幼虫;采用比色皿法、香草醛法、Folin-Ciocalteu法和亚硝酸钠-硝酸铝显色法分别测定收集的小麦籽粒阿魏酸、单宁、总酚和总黄酮含量,酶联免疫吸附法和qPCR方法分别检测收集的麦红吸浆虫幼虫GST、CarE和CYP450活性及其编码基因GST1、CarE2和CYP6A1 mRNA表达水平,分析次生物质含量与小麦对麦红吸浆虫抗性以及麦红吸浆虫解毒酶活性和基因表达的相关性。【结果】不同小麦品种（系）灌浆期籽粒阿魏酸、单宁、总酚和总黄酮含量差异明显,其中阿魏酸和单宁含量以抗虫品种科农1006最高,总酚含量以抗虫品种晋麦47最高,总黄酮含量以感虫品种西农88最高;取食不同品种（系）小麦的吸浆虫幼虫GST、CarE和CYP450活性及GST1、CarE2和CYP6A1表达水平差异亦明显,GST和CarE活性分别以取食抗虫品种科农1006和陕麦139的最高,CYP450活性以取食感虫品种小偃6号的最高;GST1和CarE2表达水平在取食抗虫品种的幼虫中均高于取食感虫品种,CYP6A1表达水平在取食抗、感性品种的幼虫中表现无规律。相关分析表明,小麦籽粒阿魏酸含量与穗被害率、粒被害率、单穗虫口和估计损失4个小麦对吸浆虫的抗性指标均呈显著负相关（P<0.05）,单宁、总酚和总黄酮含量与4个指标相关性不显著。取食不同品种（系）小麦的吸浆虫幼虫GST和CarE活性与小麦籽粒阿魏酸含量呈显著正相关,CYP450活性与单宁含量呈显著负相关（P<0.05）,总酚和总黄酮含量与3种解毒酶活性相关性不显著;GST1和CarE2表达水平分别与其GST和CarE活性呈显著正相关（P<0.05）,但CYP6A1表达水平与CYP450活性相关性不显著。【结论】阿魏酸是小麦抗麦红吸浆虫的主要次生物质,能够诱导麦红吸浆虫幼虫GST、CarE活性和相关基因的表达,它们共同作用参与麦红吸浆虫对小麦次生物质的代谢和适应。

关键词: 小麦籽粒, 次生物质, 麦红吸浆虫, 解毒酶活性, 基因表达

Abstract:

【Objective】The objective of this study is to clarify the relationship between secondary metabolite contents at grain filling stage of wheat and detoxification enzyme activities of glutathione S-transferase (GST), carboxylesterase (CarE) and cytochrome P450 (CYP450) and related gene expression in Sitodiplosis mosellena, and to explore the role of secondary metabolite in wheat resistance to S. mosellena and the metabolic mechanism.【Method】The numbers of S. mosellana larvae in wheat kernels of four resistant and four susceptible wheat varieties (lines) planted in experimental fields in Zhouzhi County, Shaanxi Province were investigated by dissecting wheat ears in May 2016. Wheat kernels at filling stage from eight varieties (lines) and S. mosellena larvae feeding wheat kernels of eight varieties (lines) were simultaneously collected. The contents of ferulic acid, tannin, total phenol and total flavonoid were determined by colorimetry, vanillin assay, Folin-Ciocalteu assay and sodium nitrite-aluminium nitrite assay, respectively. The activities of GST, CarE and CYP450 and expression levels of GST1, CarE2 and CYP6A1 in collected S. mosellena larvae were determined using enzyme linked immunosorbent assay (ELISA) and qPCR methods, respectively. And then, the relationship between secondary metabolite contents in various wheat varieties (lines) and resistance indictors of wheat to S. mosellena, as well as the interaction of secondary metabolites with detoxification enzyme activity and gene expression in S. mosellena larvae were studied by correlation analysis.【Result】The contents of ferulic acid, tannin, total phenol and total flavonoid of wheat kernel at filling stage of eight wheat varieties (lines) were significantly different. The highest contents were in the resistant variety Kenong 1006 for ferulic acid and tannin, in the resistant variety Jinmai 47 for total phenol, and in the susceptible variety Xinong 88 for total flavonoid. The activities of GST, CarE and CYP450 and expression levels of GST1, CarE2 and CYP6A1 in S. mosellena larvae from eight wheat varieties (lines) were also significantly different. The highest enzyme activities were in larvae from resistant varieties Kenong 1006 and Shaanmai 139 for GST and CarE, respectively, and from the susceptible variety Xiaoyan 6 for CYP450. The expression levels of GST1 and CarE2 were higher in larvae feeding four resistant varieties than those feeding four susceptible varieties, but CYP6A1 expression level had not obvious regularity between larvae feeding resistant and susceptible varieties. Correlation analysis results showed that the ferulic acid content of wheat kernel had significant negative correlation (P<0.05) with the four resistance indicators of wheat to S. mosellena including percentage of infested ears, percentage of infested grains, insect number per ear and estimated loss rate. There was no significant correlation between the contents of tannin, total phenol and total flavonoid and the four resistance indicators. The GST and CarE activities of S. mosellena feeding wheat kernels were significantly positively correlated to the ferulid acid content of wheat kernels, and the CYP450 activity of S. mosellena was significantly negatively correlated to the tannin content (P<0.05). No significant correlation was observed between the total phenol and total flavonoid contents of wheat kernels and the activity of any of the three detoxification enzymes. The expression levels of S. mosellena GST1 and CarE2 were significantly positively correlated with the activities of GST and CarE (P<0.05), respectively, while S. mosellena CYP6A1 expression level was not significantly related with the activity of CYP450.【Conclusion】Ferulic acid is the main secondary metabolite of wheat anti-S. mosellena, and can induce GST and CarE activities of S. mosellena larvae and related gene expression. GST and CarE jointly participate in the detoxification metabolism and adaptation of S. mosellena to wheat secondary metabolites.

Key words: wheat kernel, secondary metabolite, Sitodiplosis mosellena, detoxification enzyme activity, gene expression

陈锐,高贺,张国军,朱克岩,成卫宁. 小麦籽粒次生物质对麦红吸浆虫幼虫解毒酶活性及基因表达的影响[J]. 中国农业科学, 2020, 53(20): 4204-4214.

CHEN Rui,GAO He,ZHANG GuoJun,ZHU KeYan,CHENG WeiNing. Effects of Secondary Metabolites in Wheat Kernels on Activities of Three Detoxifying Enzymes and Related Gene Expression in Sitodiplosis mosellena[J]. Scientia Agricultura Sinica, 2020, 53(20): 4204-4214.

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引物名称 Primer name	上游引物 Forward primer (5′-3′)	下游引物 Reverse primer (5′-3′)
GST1	ATAACGGCGTGCTAATAG	AACGAGAATCCACTTGAG
CarE2	AAATGGCTCGGACTCTTTACG	ATGGCTCGGATGCTGACT
CYP6A1	TTACGAAGCGATGATGGA	GCAACTGGTGGATACTTTC
GAPDH	CCATCAAAGCAAGCAAGA	CAGCACGGAGCACAAGAC

小麦品种（系） Wheat variety (line)	穗被害率 Percentage of infested ears (%)	粒被害率 Percentage of infested grains (%)	单穗虫口数 Insect number per ear	估计损失率 Estimated loss rate (%)
陕麦139 Shaanmai 139	30.67±0.88f	3.20±0.35e	1.10±0.14f	0.42±0.05f
科农1006 Kenong 1006	50.33±1.76e	3.75±0.41e	2.30±0.27ef	1.11±0.13e
晋麦47 Jinmai 47	59.67±1.76d	5.44±0.41d	3.61±0.32de	1.80±0.15d
陕农33 Shaannong 33	69.67±2.60c	7.11±0.49c	5.07±0.39d	2.43±0.19d
小偃6号Xiaoyan 6	89.33±0.88b	11.51± 0.75b	7.57±0.53c	4.25±0.30c
西农88 Xinong 88	95.33±1.20a	12.13±0.62b	9.94±0.63b	4.97±0.29b
西农822 Xinong 822	92.00±1.53ab	12.90±0.61b	10.91±0.69b	5.02±0.29b
小偃22 Xiaoyan 22	91.33±1.86ab	15.15±0.73a	14.24±0.88a	6.12±0.36a

小麦品种（系） Wheat variety (line)	阿魏酸含量 Ferulic acid content (mg·g^-1)	单宁含量 Tannin content (mg·g^-1)	总酚含量 Total phenol content (mg·g^-1)	总黄酮含量 Total flavonoid content (mg·g^-1)
陕麦139 Shaanmai 139	6.23±0.09b	1.69±0.05b	24.64±0.85a	2.19±0.08ef
科农1006 Kenong 1006	6.57±0.10a	2.17±0.04a	23.74± 0.15a	2.94±0.06c
晋麦47 Jinmai 47	6.44±0.02ab	1.66±0.03bc	24.86±1.15a	2.67±0.05cd
陕农33 Shaannong 33	6.33±0.11ab	1.28±0.01d	12.56±0.30c	3.29±0.12b
小偃6号 Xiaoyan 6	5.51±0.16c	1.02±0.06e	23.99±1.34a	1.91±0.05f
西农88 Xinong 88	4.77±0.10d	1.55±0.02c	24.09±1.04a	3.93±0.02a
西农822 Xinong 822	4.61±0.04d	1.12±0.01e	14.55±0.61bc	2.39±0.15de
小偃22 Xiaoyan 22	5.72±0.15c	1.55±0.05c	15.83±1.25b	3.44±0.06b

次生物质 Secondary metabolite	穗被害率 Percentage of infested ears		粒被害率 Percentage of infested grains		单穗虫口数 Insect number per ear		估计损失率 Estimated loss rate
次生物质 Secondary metabolite	r	P	r	P	r	P	r	P
阿魏酸 Ferulic acid	-0.774	0.024*	-0.778	0. 023*	-0.726	0.041*	-0.774	0.024*
单宁 Tannin	-0.620	0.101	-0.597	0.118	-0.477	0.232	-0.550	0.158
总黄酮Total flavonoid	0.332	0.422	0.275	0.509	0.378	0.356	0.337	0.415
总酚 Total phenol	-0.392	0.337	-0.438	0.278	-0.495	0.212	-0.426	0.292

小麦品种（系） Wheat variety (line)	GST活性 GST activity (U/mg protein)	CarE 活性 CarE activity (U/mg protein)	CYP450活性 CYP450 activity (U/mg protein)
陕麦139 Shaanmai 139	0.1633±0.0185bcd	0.2284±0.0054a	0.1446±0.0173bc
科农1006 Kenong 1006	0.2144±0.012a	0.1823±0.0103b	0.1124±0.0046c
晋麦47 Jinmai 47	0.1707±0.0242abc	0.1414±0.0087c	0.1248±0.0107c
陕农33 Shaannong 33	0.2038±0.0177ab	0.2116±0.0135a	0.1163±0.0065c
小偃6号 Xiaoyan 6	0.1913±0.0022ab	0.1784±0.0079b	0.1885±0.0038a
西农88 Xinong 88	0.0963±0.0055e	0.1016±0.0071d	0.1304±0.0143c
西农822 Xinong 822	0.1206 ±0.0101de	0.1074±0.0037d	0.1791±0.0217ab
小偃22 Xiaoyan 22	0.1333±0.0064cde	0.1242±0.0038cd	0.1306±0.0001c