Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (<i>Sitobion avenae</i>)

Benzoxazinoids are important secondary metabolites in gramineae plants and have inhibitory and toxic effects against a wide range of herbivore pests. However, the relationship between benzoxazinoid level and plant resistance to aphids remains controversial. In this study, we investigated the relatio...

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Main Authors: Zhanfeng Zhang, Hao Lan, Hehe Cao, Xiangshun Hu, Yongliang Fan, Yue Song, Lijuan Wu, Tong-Xian Liu
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:Metabolites
Subjects:
Online Access:https://www.mdpi.com/2218-1989/11/11/783
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author Zhanfeng Zhang
Hao Lan
Hehe Cao
Xiangshun Hu
Yongliang Fan
Yue Song
Lijuan Wu
Tong-Xian Liu
author_facet Zhanfeng Zhang
Hao Lan
Hehe Cao
Xiangshun Hu
Yongliang Fan
Yue Song
Lijuan Wu
Tong-Xian Liu
author_sort Zhanfeng Zhang
collection DOAJ
description Benzoxazinoids are important secondary metabolites in gramineae plants and have inhibitory and toxic effects against a wide range of herbivore pests. However, the relationship between benzoxazinoid level and plant resistance to aphids remains controversial. In this study, we investigated the relationship between benzoxazinoids composition and concentration in wheat leaves and the resistance to the grain aphid <i>Sitobion avenae</i>. Overall, six benzoxazinoids were detected and identified by mass spectrometry based metabolites profiling, including three lactams, two hydroxamic acids, and one methyl derivative. The constitutive levels of these benzoxazinoids were significantly different among the wheat varieties/lines. However, none of these benzoxazinoids exhibited considerable correlation with aphid resistance. <i>S</i><i>. avenae</i> feeding elevated the level of 2-<i>O</i>-<i>β</i>-D-glucopyranosyloxy-4,7-dimethoxy-(2H)-1,4-benzoxazin-3(4H)-one (HDMBOA-Glc) and reduced the level of 2-<i>O</i>-<i>β</i>-D-glucopyranosyloxy-4-hydroxy-7-(2H)-methoxy-1,4-benzoxazin-3(4H)-one (DIMBOA-Glc) in some of the wheat varieties/lines. Moreover, aphid-induced level of DIMBOA-Glc was positively related with callose deposition, which was closely associated with aphid resistance. Wheat leaves infiltrated with DIMBOA-Glc caused a noticeable increase of callose deposition and the effect was in a dose dependent manner. This study suggests that the constitutive level of benzoxazinoids has limited impact on <i>S. avenae</i>. Aphid feeding can affect the balance of benzoxazinoids metabolism and the dynamic level of benzoxazinoids can act as a signal of callose deposition for <i>S. avenae</i> resistance. This study will extend our understanding of aphid–wheat interaction and provides new insights in aphid-resistance wheat breeding.
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spelling doaj.art-9e7f87030f954928a05722de965cb5022023-11-23T00:21:29ZengMDPI AGMetabolites2218-19892021-11-01111178310.3390/metabo11110783Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (<i>Sitobion avenae</i>)Zhanfeng Zhang0Hao Lan1Hehe Cao2Xiangshun Hu3Yongliang Fan4Yue Song5Lijuan Wu6Tong-Xian Liu7State Key Laboratory of Crop Stress Biology in Arid Areas, Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, College of Plant protection, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, College of Plant protection, Northwest A&F University, Yangling 712100, ChinaCollege of Plant Health and Medicine, Qingdao Agricultural University, Qingdao 266109, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, College of Plant protection, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, College of Plant protection, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, College of Plant protection, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, College of Plant protection, Northwest A&F University, Yangling 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, College of Plant protection, Northwest A&F University, Yangling 712100, ChinaBenzoxazinoids are important secondary metabolites in gramineae plants and have inhibitory and toxic effects against a wide range of herbivore pests. However, the relationship between benzoxazinoid level and plant resistance to aphids remains controversial. In this study, we investigated the relationship between benzoxazinoids composition and concentration in wheat leaves and the resistance to the grain aphid <i>Sitobion avenae</i>. Overall, six benzoxazinoids were detected and identified by mass spectrometry based metabolites profiling, including three lactams, two hydroxamic acids, and one methyl derivative. The constitutive levels of these benzoxazinoids were significantly different among the wheat varieties/lines. However, none of these benzoxazinoids exhibited considerable correlation with aphid resistance. <i>S</i><i>. avenae</i> feeding elevated the level of 2-<i>O</i>-<i>β</i>-D-glucopyranosyloxy-4,7-dimethoxy-(2H)-1,4-benzoxazin-3(4H)-one (HDMBOA-Glc) and reduced the level of 2-<i>O</i>-<i>β</i>-D-glucopyranosyloxy-4-hydroxy-7-(2H)-methoxy-1,4-benzoxazin-3(4H)-one (DIMBOA-Glc) in some of the wheat varieties/lines. Moreover, aphid-induced level of DIMBOA-Glc was positively related with callose deposition, which was closely associated with aphid resistance. Wheat leaves infiltrated with DIMBOA-Glc caused a noticeable increase of callose deposition and the effect was in a dose dependent manner. This study suggests that the constitutive level of benzoxazinoids has limited impact on <i>S. avenae</i>. Aphid feeding can affect the balance of benzoxazinoids metabolism and the dynamic level of benzoxazinoids can act as a signal of callose deposition for <i>S. avenae</i> resistance. This study will extend our understanding of aphid–wheat interaction and provides new insights in aphid-resistance wheat breeding.https://www.mdpi.com/2218-1989/11/11/783benzoxazinoidswheat<i>Sitobion avenae</i>mass spectrometryaphid resistancecallose deposition
spellingShingle Zhanfeng Zhang
Hao Lan
Hehe Cao
Xiangshun Hu
Yongliang Fan
Yue Song
Lijuan Wu
Tong-Xian Liu
Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (<i>Sitobion avenae</i>)
Metabolites
benzoxazinoids
wheat
<i>Sitobion avenae</i>
mass spectrometry
aphid resistance
callose deposition
title Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (<i>Sitobion avenae</i>)
title_full Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (<i>Sitobion avenae</i>)
title_fullStr Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (<i>Sitobion avenae</i>)
title_full_unstemmed Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (<i>Sitobion avenae</i>)
title_short Impacts of Constitutive and Induced Benzoxazinoids Levels on Wheat Resistance to the Grain Aphid (<i>Sitobion avenae</i>)
title_sort impacts of constitutive and induced benzoxazinoids levels on wheat resistance to the grain aphid i sitobion avenae i
topic benzoxazinoids
wheat
<i>Sitobion avenae</i>
mass spectrometry
aphid resistance
callose deposition
url https://www.mdpi.com/2218-1989/11/11/783
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