Transcriptome analysis of aphid-resistant and susceptible near isogenic lines reveals candidate resistance genes in cowpea (Vigna unguiculata)

Abstract Background Cowpea (Vigna unguiculata) is a crucial crop for regions of the world that are prone to both heat and drought; however, the phytotoxic cowpea aphid (Aphis craccivora) impairs plant physiology at low population levels. Both antibiotic and antixenotic forms of resistance to the aph...

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Main Authors: Jacob R. MacWilliams, Paul D. Nabity, Kerry E. Mauck, Isgouhi Kaloshian
Format: Article
Language:English
Published: BMC 2023-01-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-022-04021-w
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author Jacob R. MacWilliams
Paul D. Nabity
Kerry E. Mauck
Isgouhi Kaloshian
author_facet Jacob R. MacWilliams
Paul D. Nabity
Kerry E. Mauck
Isgouhi Kaloshian
author_sort Jacob R. MacWilliams
collection DOAJ
description Abstract Background Cowpea (Vigna unguiculata) is a crucial crop for regions of the world that are prone to both heat and drought; however, the phytotoxic cowpea aphid (Aphis craccivora) impairs plant physiology at low population levels. Both antibiotic and antixenotic forms of resistance to the aphid have been mapped to two quantitative trait loci (QTLs) and near isogenic lines (NILs). The molecular mechanism for this resistance response remains unknown. Results To understand the genes underlying susceptibility and resistance, two cowpea lines with shared heritage were infested along a time course and characterized for transcriptome variation. Aphids remodeled cowpea development and signaling relative to host plant resistance and the duration of feeding, with resource acquisition and mobilization determining, in part, susceptibility to aphid attack. Major differences between the susceptible and resistant cowpea were identified including two regions of interest housing the most genetic differences between the lines. Candidate genes enabling aphid resistance include both conventional resistance genes (e.g., leucine rich repeat protein kinases) as well as multiple novel genes with no known orthologues. Conclusions Our results demonstrate that feeding by the cowpea aphid globally remodels the transcriptome of cowpea, but how this occurs depends on both the duration of feeding and host-plant resistance. Constitutive expression profiles of the resistant genotype link aphid resistance to a finely-tuned resource management strategy that ultimately reduces damage (e.g., chlorosis) and delays cell turnover, while impeding aphid performance. Thus, aphid resistance in cowpea is a complex, multigene response that involves crosstalk between primary and secondary metabolism.
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spelling doaj.art-a48d65aa32d745dd8f195c7a6d00e2142023-01-15T12:08:04ZengBMCBMC Plant Biology1471-22292023-01-0123111710.1186/s12870-022-04021-wTranscriptome analysis of aphid-resistant and susceptible near isogenic lines reveals candidate resistance genes in cowpea (Vigna unguiculata)Jacob R. MacWilliams0Paul D. Nabity1Kerry E. Mauck2Isgouhi Kaloshian3Graduate Program in Biochemistry and Molecular Biology, University of California RiversideDepartment of Botany and Plant Sciences, University of California RiversideInstitute for Integrative Genome Biology, University of California RiversideGraduate Program in Biochemistry and Molecular Biology, University of California RiversideAbstract Background Cowpea (Vigna unguiculata) is a crucial crop for regions of the world that are prone to both heat and drought; however, the phytotoxic cowpea aphid (Aphis craccivora) impairs plant physiology at low population levels. Both antibiotic and antixenotic forms of resistance to the aphid have been mapped to two quantitative trait loci (QTLs) and near isogenic lines (NILs). The molecular mechanism for this resistance response remains unknown. Results To understand the genes underlying susceptibility and resistance, two cowpea lines with shared heritage were infested along a time course and characterized for transcriptome variation. Aphids remodeled cowpea development and signaling relative to host plant resistance and the duration of feeding, with resource acquisition and mobilization determining, in part, susceptibility to aphid attack. Major differences between the susceptible and resistant cowpea were identified including two regions of interest housing the most genetic differences between the lines. Candidate genes enabling aphid resistance include both conventional resistance genes (e.g., leucine rich repeat protein kinases) as well as multiple novel genes with no known orthologues. Conclusions Our results demonstrate that feeding by the cowpea aphid globally remodels the transcriptome of cowpea, but how this occurs depends on both the duration of feeding and host-plant resistance. Constitutive expression profiles of the resistant genotype link aphid resistance to a finely-tuned resource management strategy that ultimately reduces damage (e.g., chlorosis) and delays cell turnover, while impeding aphid performance. Thus, aphid resistance in cowpea is a complex, multigene response that involves crosstalk between primary and secondary metabolism.https://doi.org/10.1186/s12870-022-04021-wHerbivoryQTLAntibiosisAntixenosisLegume
spellingShingle Jacob R. MacWilliams
Paul D. Nabity
Kerry E. Mauck
Isgouhi Kaloshian
Transcriptome analysis of aphid-resistant and susceptible near isogenic lines reveals candidate resistance genes in cowpea (Vigna unguiculata)
BMC Plant Biology
Herbivory
QTL
Antibiosis
Antixenosis
Legume
title Transcriptome analysis of aphid-resistant and susceptible near isogenic lines reveals candidate resistance genes in cowpea (Vigna unguiculata)
title_full Transcriptome analysis of aphid-resistant and susceptible near isogenic lines reveals candidate resistance genes in cowpea (Vigna unguiculata)
title_fullStr Transcriptome analysis of aphid-resistant and susceptible near isogenic lines reveals candidate resistance genes in cowpea (Vigna unguiculata)
title_full_unstemmed Transcriptome analysis of aphid-resistant and susceptible near isogenic lines reveals candidate resistance genes in cowpea (Vigna unguiculata)
title_short Transcriptome analysis of aphid-resistant and susceptible near isogenic lines reveals candidate resistance genes in cowpea (Vigna unguiculata)
title_sort transcriptome analysis of aphid resistant and susceptible near isogenic lines reveals candidate resistance genes in cowpea vigna unguiculata
topic Herbivory
QTL
Antibiosis
Antixenosis
Legume
url https://doi.org/10.1186/s12870-022-04021-w
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