AcDCXR Is a Cowpea Aphid Effector With Putative Roles in Altering Host Immunity and Physiology

Jacob R MacWilliams; Stephanie Dingwall; Quentin Chesnais; Akiko Sugio; Isgouhi Kaloshian

doi:10.3389/fpls.2020.00605

AcDCXR Is a Cowpea Aphid Effector With Putative Roles in Altering Host Immunity and Physiology

Front Plant Sci. 2020 May 15:11:605. doi: 10.3389/fpls.2020.00605. eCollection 2020.

Authors

Jacob R MacWilliams¹, Stephanie Dingwall², Quentin Chesnais³, Akiko Sugio⁴, Isgouhi Kaloshian^{1

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Affiliations

¹ Graduate Program in Biochemistry and Molecular Biology, University of California, Riverside, Riverside, CA, United States.
² Department of Biochemistry, University of California, Riverside, Riverside, CA, United States.
³ Université de Strasbourg, INRAE, SVQV UMR-A1131, Colmar, France.
⁴ INRAE, UMR1349, Institute of Genetics, Environment and Plant Protection, Le Rheu, France.
⁵ Department of Nematology, University of California Riverside, Riverside, CA, United States.
⁶ Institute for Integrative Genome Biology, University of California, Riverside, Riverside, CA, United States.

Abstract

Cowpea, Vigna unguiculata, is a crop that is essential to semiarid areas of the world like Sub-Sahara Africa. Cowpea is highly susceptible to cowpea aphid, Aphis craccivora, infestation that can lead to major yield losses. Aphids feed on their host plant by inserting their hypodermal needlelike flexible stylets into the plant to reach the phloem sap. During feeding, aphids secrete saliva, containing effector proteins, into the plant to disrupt plant immune responses and alter the physiology of the plant to their own advantage. Liquid chromatography tandem mass spectrometry (LC-MS/MS) was used to identify the salivary proteome of the cowpea aphid. About 150 candidate proteins were identified including diacetyl/L-xylulose reductase (DCXR), a novel enzyme previously unidentified in aphid saliva. DCXR is a member of short-chain dehydrogenases/reductases with dual enzymatic functions in carbohydrate and dicarbonyl metabolism. To assess whether cowpea aphid DCXR (AcDCXR) has similar functions, recombinant AcDCXR was purified and assayed enzymatically. For carbohydrate metabolism, the oxidation of xylitol to xylulose was tested. The dicarbonyl reaction involved the reduction of methylglyoxal, an α-β-dicarbonyl ketoaldehyde, known as an abiotic and biotic stress response molecule causing cytotoxicity at high concentrations. To assess whether cowpea aphids induce methylglyoxal in plants, we measured methylglyoxal levels in both cowpea and pea (Pisum sativum) plants and found them elevated transiently after aphid infestation. Agrobacterium-mediated transient overexpression of AcDCXR in pea resulted in an increase of cowpea aphid fecundity. Taken together, our results indicate that AcDCXR is an effector with a putative ability to generate additional sources of energy to the aphid and to alter plant defense responses. In addition, this work identified methylglyoxal as a potential novel aphid defense metabolite adding to the known repertoire of plant defenses against aphid pests.

Keywords: DCXR; cowpea aphid; diacetyl/L-xylulose reductase; effector; host defense; methylglyoxal; salivary proteins.