Impact of Mutations in Arabidopsis thaliana Metabolic Pathways on Polerovirus Accumulation, Aphid Performance, and Feeding Behavior.

Florent Bogaert,Aurélie Marmonier,Claire Villeroy,Elodie Pichon,Sylvaine Boissinot,Quentin Chesnais,Véronique Ziegler-Graff,Martin Drucker,Véronique Brault

doi:10.3390/v12020146

Abstract

During the process of virus acquisition by aphids, plants respond to both the virus and the aphids by mobilizing different metabolic pathways. It is conceivable that the plant metabolic responses to both aggressors may be conducive to virus acquisition. To address this question, we analyze the accumulation of the phloem-limited polerovirus Turnip yellows virus (TuYV), which is strictly transmitted by aphids, and aphid’s life traits in six Arabidopsis thaliana mutants (xth33, ss3-2, nata1, myc234, quad, atr1D, and pad4-1). We observed that mutations affecting the carbohydrate metabolism, the synthesis of a non-protein amino acid and the glucosinolate pathway had an effect on TuYV accumulation. However, the virus titer did not correlate with the virus transmission efficiency. Some mutations in A. thaliana affect the aphid feeding behavior but often only in infected plants. The duration of the phloem sap ingestion phase, together with the time preceding the first sap ingestion, affect the virus transmission rate more than the virus titer did. Our results also show that the aphids reared on infected mutant plants had a reduced biomass regardless of the mutation and the duration of the sap ingestion phase.

Highlights

Aphids are a large group of Hemipteran insects that induce direct damage on plants but are, more importantly, major vectors of plant viruses
Arabidopsis thaliana mutant seeds were obtained from stock centers for pad4-1
The nata1 mutant contains a mutation in a gene controlling the synthesis of a non-protein amino acid, Nδ -acetylornithine, which negatively impacts M. persicae when aphids acquire it from artificial medium or from plant leaves transiently expressing NATA1 [46]

Summary

Introduction

Aphids are a large group of Hemipteran insects that induce direct damage on plants but are, more importantly, major vectors of plant viruses. Once an aphid probes and feeds on a host plant, it releases salivary secretions that are recognized and elicit plant defenses [2,3,4,5]. These reactions implement a number of metabolic and physiological modifications that may have a detrimental effect on aphids [6,7,8,9]. Several hormonal pathways induced in reaction to M. persicae are characterized in A. thaliana and involve ethylene, salicylic, jasmonic, and abscisic acid-signaling pathways [7,8]. PAD4 (phytoalexin-deficient 4) and PAD3, a cytochrome P450 involved in the synthesis of camalexin, both act as key players in modulating plant

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Discussion

Conclusion