Arabidopsis MATE45 antagonizes local abscisic acid signaling to mediate development and abiotic stress responses

Abstract

Anthocyanins provide ideal visual markers for the identification of mutations that disrupt molecular responses to abiotic stress. We screened Arabidopsis mutants of ABC (ATP-Binding Cassette) and MATE (Multidrug And Toxic compound Extrusion) transporter genes under nutritional stress and identified four genes (ABCG25, ABCG9, ABCG5, and MATE45) required for normal anthocyanin pigmentation. ABCG25 was previously demonstrated to encode a vascular-localized cellular exporter of abscisic acid (ABA). Our results show that MATE45 encodes an aerial meristem- and a vascular-localized transporter associated with the trans-Golgi, and that it plays an important role in controlling the levels and distribution of ABA in growing aerial meristems and non-meristematic tissues. MATE45 promoter-GUS reporter fusions revealed the activity localized to the leaf and influorescence meristems and the vasculature. Loss-of-function mate45 mutants exhibited accelerated rates of aerial organ initiation suggesting at least partial functional conservation with the maize ortholog bige1. The aba2-1 mutant, which is deficient in ABA biosynthesis, exhibited a number of phenotypes that were rescued in the mate45-1 aba2-1 double mutant. mate45 exhibited enhanced the seed dormancy, and germination was hypersensitive to ABA. Enhanced frequency of leaf primordia growth in mate45 seedlings grown in nutrient imbalance stress was ABA-dependent. The ABA signaling reporter construct pRD29B::GUS revealed elevated levels of ABA signaling in the true leaf primordia of mate45 seedlings grown under nutritional stress, and gradually reduced signaling in surrounding cotyledon and hypocotyl tissues concomitant with reduced expressions of ABCG25. Our results suggest a role of MATE45 in reducing meristematic ABA and in maintaining ABA distribution in adjacent non-meristematic tissues.