The Role of UV-B light on Small RNA Activity During Grapevine Berry Development

• Published in: G3 : genes - genomes - genetics 2019-03, Vol.9 (3), p.769-787
• Main Authors: Sunitha, Sukumaran, Loyola, Rodrigo, Alcalde, José Antonio, Arce-Johnson, Patricio, Matus, José Tomás, Rock, Christopher D
• Format: Article
• Language: English
• Subjects: anthocyanin; Anthocyanins - biosynthesis; Arabidopsis; Argonaute Proteins - metabolism; Fruit - genetics; Fruit - metabolism; Fruit - radiation effects; Gene Expression Profiling; Gene Expression Regulation, Developmental; Gene Expression Regulation, Plant; Investigations; light signaling; MicroRNAs - genetics; MicroRNAs - metabolism; miRNAs; MYBA; Oxidative Stress; Plant Proteins - metabolism; polyphenols; RNA, Plant - genetics; RNA, Plant - metabolism; Signal Transduction; siRNAs; Ultraviolet Rays; veraison; Vitis - genetics; Vitis - metabolism; Vitis - radiation effects
• ISSN: 2160-1836; 2160-1836
• DOI: 10.1534/g3.118.200805

Abstract We explored the effects of ultraviolet B radiation (UV-B) on the developmental dynamics of microRNAs and phased small-interfering-RNA (phasi-RNAs)-producing loci by sequencing small RNAs in vegetative and reproductive organs of grapevine (Vitis vinifera L.). In particular, we tested different UV-B conditions in in vitro-grown plantlets (high-fluence exposition) and in berries from field-grown (radiation filtering) and greenhouse-grown (low- and high-fluence expositions) adult plants throughout fruit development and ripening. The functional significance of the observed UV-coordinated miRNA responses was supported by degradome evidences of ARGONAUTE (AGO)-programmed slicing of mRNAs. Co-expression patterns of the up-regulated miRNAs miR156, miR482, miR530, and miR828 with cognate target gene expressions in response to high-fluence UV-B was tested by q-RT-PCR. The observed UV-response relationships were also interrogated against two published UV-stress and developmental transcriptome datasets. Together, the dynamics observed between miRNAs and targets suggest that changes in target abundance are mediated transcriptionally and, in some cases, modulated post-transcriptionally by miRNAs. Despite the major changes in target abundance are being controlled primarily by those developmental effects that are similar between treatments, we show evidence for novel miRNA-regulatory networks in grape. A model is proposed where high-fluence UV-B increases miR168 and miR530 that target ARGONAUTE 1 (AGO1) and a Plus-3 domain mRNA, respectively, while decreasing miR403 that targets AGO2, thereby coordinating post-transcriptional gene silencing activities by different AGOs. Up-regulation of miR3627/4376 could facilitate anthocyanin accumulation by antagonizing a calcium effector, whereas miR395 and miR399, induced by micronutrient deficiencies known to trigger anthocyanin accumulation, respond positively to UV-B radiation. Finally, increases in the abundance of an anthocyanin-regulatory MYB-bHLH-WD40 complex elucidated in Arabidopsis, mediated by UV-B-induced changes in miR156/miR535, could contribute to the observed up-regulation of miR828. In turn, miR828 would regulate the AtMYB113-ortologues MYBA5, A6 and A7 (and thereby anthocyanins) via a widely conserved and previously validated auto-regulatory loop involving miR828 and phasi TAS4abc RNAs.