Characterization of wheat (Triticum aestivum) TIFY family and role of Triticum Durum TdTIFY11a in salt stress tolerance

RESEARCH ARTICLE Characterization of wheat (Triticum aestivum) TIFY family and role of Triticum Durum TdTIFY11a in salt stress tolerance Chantal Ebel1, Asma BenFeki1, Moez Hanin1, Roberto Solano2, Andrea Chini2* 1 Plant Physiology and Functional Genomics Research Unit, Institute of Biotechnology, University of Sfax, BP Sfax, Tunisia, 2 Plant Molecular Genetics Department, Centro Nacional de Biotecnologı́a, Consejo Superior de Investigaciones Cientı́ficas (CNB-CSIC), Madrid, Spain a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Ebel C, BenFeki A, Hanin M, Solano R, Chini A (2018) Characterization of wheat (Triticum aestivum) TIFY family and role of Triticum Durum TdTIFY11a in salt stress tolerance. PLoS ONE 13 (7): e0200566. https://doi.org/10.1371/journal. pone.0200566 Editor: Jin-Song Zhang, Institute of Genetics and Developmental Biology Chinese Academy of Sciences, CHINA Received: March 20, 2018 Accepted: June 28, 2018 Published: July 18, 2018 Copyright: © 2018 Ebel et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are available within the manuscript and its Supporting Information files. Funding: This work was supported by: 1) grant BIO2016-77216-R of the Spanish Ministry for Science and Innovation (MINECO-AEI/FEDER) to RS and AC (http://www.idi.mineco.gob.es/portal/ site/MICINN?lang_choosen=en); 2) grant iCOOP+ 2013/COOPB20060 of the Consejo Superior de Investigaciones Cientı́ficas to AC and CE (http:// * Abstract The TIFY proteins constitute a plant-specific super-family and they are involved in regulating many plant processes, such as development, defences and stress responses. The Jasmonate-ZIM-Domain (JAZ) proteins, the best-characterized sub-group of the TIFY family are key regulator of the jasmonic acid (JA) signalling pathway. Jasmonates regulate several aspects of plant development, and play a primary role in defence mechanisms as well as in plant responses to abiotic stresses. The TIFY family is well studied in dicots but poorly investigated in monocots. The present study reports an extensive genomic identification of TIFY proteins from Triticum aestivum. We identified 49 TIFY genes, which were annotated according to three sub-genomes (AABBDD) of T. aestivum. Following their clustering with Oryza sativa and Brachypodium distachyon, the 49 genes were grouped in 18 different TIFY homeologous subsets. Expression analyses of 6 representative TIFY genes on Tunisian durum wheat seedlings revealed their differential regulation by various stress treatment, including JA, ABA and salt stress. TIFY11a was specifically induced after salt treatment. Transgenic lines over-expressing TdTIFY11a showed higher germination and growth rates under high salinity conditions, compared to wild type plants. In summary, our results outline a relevant role of wheat TIFY proteins in promoting germination under salt stress. Introduction Because of their sessile lifestyle, plants have evolved myriads of defense mechanisms to survive the continuous challenges of their ever-changing environment, including exposure to pathogens and insects but also, droughts, salty soils or mineral deficiency. Many signaling pathways participate in plant adaptation to environmental cues. Plant hormones are major actors of plant defense against environmental changes and among them abscisic acid (ABA) is considered as the abiotic stress hormone while jasmonic acid (JA) is traditionally regarded as the hormone that regulates plant defenses to necrotrophic pathogens, fungi, insect and nematodes[1–3]. The basic signaling mechanisms orchestrating JA-responses have been deciphered[2,4]. In response to stresses or endogenous signals, plants accumulate the active form of the hormone, (+)-7-iso-JA-Ile (JA-Ile), the ligand of the co-receptor complex formed by the F-box protein PLOS ONE | https://doi.org/10.1371/journal.pone.0200566 July 18, 2018 1 / 18 Role of wheat TIFY genes in salt stress tolerance www.csic.es/i-coop); 3) grant AP/040886/11 from the (AECID) to AC (http://www.aecid.es/EN/aecid); 4) Science by Woman grant from “Mujeres por Africa” Foundation to CE (https://www. mujeresporafrica.es/en/content/science-women); 5) grant from the Tunisian Higher Ministry of Education to CE and MH (http://www.fundit.fr/en/ institutions/ministry-higher-education-andscientific-research-tunisia-mesrs). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. coronatine-insensitive 1 (COI1) and the co-receptor Jasmonate ZIM-domain (JAZ)[5,6]. The JA-Ile-mediated COI1-JAZ interaction promotes the ubiquitination and degradation of the JAZ repressors that liberates several transcription factors (TFs) including the JA master regulator MYC2[7–9], a basic helix-loop-helix (bHLH) DNA-binding protein. In turn, these TFs trigger JA-specific cellular outputs such as defense responses or inhibition of plant growth [2,4]. The conserved Jas domain of the JAZ repressors mediates the interaction with MYC2, but also with other TFs of different families such as other bHLHs, MYBs, YABBYs, WRKY, AP2 and EIN3/EIL3[1,2,4]. In addition, alternative splicing, resulting in the retention of the Jas-intron, encodes truncated JAZ variants that act as constitutive repressors of the JA-pathway, such as the case of the Arabidopsis JAZ10.4[10–12]. Additional truncated JAZ variants lacking the Jas motif also confer dominant insensitivity to JA[4,10,12]. All JAZ proteins retain the conserved ZIM (Zinc-finger expressed in Inflorescence Meristems) or TIFY domain, and therefore they belong to the plant specific family called TIFY family that includes JAZ, TIFY8, ZIM-like (ZML) and PEAPOD (PPD) proteins which have been particularly well studied in Arabidopsis[13]. These Arabidopsis proteins all possess a conserved TIFY or ZIM domain composed of 36 amino acids containing a core motif TIF[F/Y]XG[13]. The TIFY domain is required for JAZ dimerization and mediates the interaction with NINJA (Novel Interactor of JAZ), which recruits the TOPLESS (TPL) general transcriptional corepressor[11,14,15]. In addition to the TIFY domain, ZMLs possess a C2C2-GATA zinc-finger DNA-binding domain and a CCT-domain (CONSTANS, CO-like, TOC1) that is closely related to the Jas domain in JAZ proteins[16]. In contrast, the PPD proteins, beside the TIFY domain, harbor at their N-terminus a typical PPD domain[13,17]. Some TIFY proteins, such as AtJAZ7 and AtJAZ8, hold an EAR motif (ethylene-responsive element binding factor-associated amphiphilic repression) that enables them to directly recruit the TPL co-repressor[18]. Beyond Arabidopsis, TIFY families have (...truncated)