Iron deficiency triggered transcriptome changes in bread wheat

Comput Struct Biotechnol J. 2020 Sep 20:18:2709-2722. doi: 10.1016/j.csbj.2020.09.009. eCollection 2020.

Abstract

A series of complex transport, storage and regulation mechanisms control iron metabolism and thereby maintain iron homeostasis in plants. Despite several studies on iron deficiency responses in different plant species, these mechanisms remain unclear in the allohexaploid wheat, which is the most widely cultivated commercial crop. We used RNA sequencing to reveal transcriptomic changes in the wheat flag leaves and roots, when subjected to iron limited conditions. We identified 5969 and 2591 differentially expressed genes (DEGs) in the flag leaves and roots, respectively. Genes involved in the synthesis of iron ligands i.e., nicotianamine (NA) and deoxymugineic acid (DMA) were significantly up-regulated during iron deficiency. In total, 337 and 635 genes encoding transporters exhibited altered expression in roots and flag leaves, respectively. Several genes related to MAJOR FACILITATOR SUPERFAMILY (MFS), ATP-BINDING CASSETTE (ABC) transporter superfamily, NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN (NRAMP) family and OLIGOPEPTIDE TRANSPORTER (OPT) family were regulated, indicating their important roles in combating iron deficiency stress. Among the regulatory factors, the genes encoding for transcription factors of BASIC HELIX-LOOP-HELIX (bHLH) family were highly up-regulated in both roots and the flag leaves. The jasmonate biosynthesis pathway was significantly altered but with notable expression differences between roots and flag leaves. Homoeologs expression and induction bias analysis revealed subgenome specific differential expression. Our findings provide an integrated overview on regulated molecular processes in response to iron deficiency stress in wheat. This information could potentially serve as a guideline for breeding iron deficiency stress tolerant crops as well as for designing appropriate wheat iron biofortification strategies.

Keywords: 3-HMA, 3-hydroxymugineic acid; ABC, ATP-BINDING CASSETTE; ACC, 1-aminocyclopropane-1-carboxylate; AEC, AUXIN EFFLUX CARRIER; AOC, ALLENE OXIDE CYCLASE; AOS, ALLENE OXIDE SYNTHASE; AQP, AQUAPORIN; AVA, avenic acid; DEGs, differentially expressed genes; DMA, deoxymugineic acid; DMAS, DEOXYMUGINEIC ACID SYNTHASE; DPA, days post anthesis; ERF, ETHYLENE-RESPONSIVE FACTOR; FAD, FATTY ACID DESATURASE; FDR, false discovery rate; FIT, FER-LIKE IRON DEFICIENCY-INDUCED TRANSCRIPTION FACTOR; FRO, FERRIC REDUCTASE OXIDASE; GCN, gene co-expression network; GO, Gene ontology; GSH, GLUTATHIONE; HC, high confidence; HMA, HEAVY METAL-ASSOCIATED; IDE, iron deficiency-responsive cis-acting element; IDEF, IDE BINDING FACTOR; IHW, independent hypothesis weighting; ILR3, IAA‐LEUCINE RESISTANT3; IREG/FPN, IRON REGULATED PROTEIN/FERROPORTIN; IRT1, IRON-REGULATED TRANSPORTER; Iron deficiency; Iron, Fe; JAs, jasmonates; JMT, JASMONATE O-METHYLTRANSFERASE; KAT, 3-KETOACYL-COA THIOLASE; LOX, LIPOXYGENASE; MA, mugineic acid; MATE, MULTI ANTIMICROBIAL EXTRUSION PROTEIN; MFS, MAJOR FACILITATOR SUPERFAMILY; MRP, MULTIDRUG RESISTANCE PROTEIN; MT, METALLOTHIONEIN; NA, nicotianamine; NAAT, NICOTIANAMINE AMINOTRANSFERASE; NAC, NO APICAL MERISTEM (NAM)/ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR (ATAF)/CUP-SHAPED COTYLEDON (CUC); NAS, NICOTIANAMINE SYNTHASE; NRAMP, NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN; NRT1/PTR, NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER; OPCL, 4-COUMARATE COA LIGASE; OPR, 12-OXOPHYTODIENOATE REDUCTASE; OPT, OLIGOPEPTIDE TRANSPORTER; PDR, PLEIOTROPIC DRUG RESISTANCE; PLA, PHOSPHOLIPASE A1; PRI, POSITIVE REGULATOR OF IRON DEFICIENCY RESPONSE; PSs, phytosiderophores; PT, peptide transport; PYE, POPEYE; RNA sequencing; SAM, S-adenosyl-L-methionine; SAMS, S-ADENOSYL-L-METHIONINE SYNTHETASE; SLC40A1, SOLUTE CARRIER FAMILY 40 MEMBER 1; SWEET, SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTERS; TOM, TRANSPORTER OF MUGINEIC ACID; Transcriptomic profiles; VIT, VACUOLAR IRON TRANSPORTER; Wheat; YSL, YELLOW STRIPE LIKE; ZIFL, ZINC INDUCED FACILITATOR-LIKE; ZIP, ZINC/IRON PERMEASE; bHLH, BASIC HELIX-LOOP-HELIX; bZIP, BASIC LEUCINE ZIPPER; epiHDMA, 3-epihydroxy-2′-deoxymugineic acid; epiHMA, 3-epihydroxymugineic acid.