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      Interaction between row‐type genes in barley controls meristem determinacy and reveals novel routes to improved grain

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          Summary

          • Hordeum species develop a central spikelet flanked by two lateral spikelets at each inflorescence node. In ‘two‐rowed’ spikes, the central spikelet alone is fertile and sets grain, while in ‘six‐rowed’ spikes, lateral spikelets can also produce grain. Induced loss‐of‐function alleles of any of five Six‐rowed spike ( VRS ) genes ( VRS1‐5 ) cause complete to intermediate gains of lateral spikelet fertility. Current six‐row cultivars contain natural defective vrs1 and vrs5 alleles. Little information is known about VRS mechanism(s).

          • We used comparative developmental, expression and genetic analyses on single and double vrs mutants to learn more about how VRS genes control development and assess their agronomic potential.

          • We show that all VRS genes repress fertility at carpel and awn emergence in developing lateral spikelets. VRS4, VRS3 and VRS5 work through VRS1 to suppress fertility, probably by inducing VRS1 expression. Pairing vrs3, vrs4 or vrs5 alleles increased lateral spikelet fertility, despite the presence of a functional VRS1 allele. The vrs3 allele caused loss of spikelet identity and determinacy, improved grain homogeneity and increased tillering in a vrs4 background, while with vrs5, decreased tiller number and increased grain weight.

          • Interactions amongst VRS genes control spikelet infertility, determinacy and outgrowth, and novel routes to improving six‐row grain.

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          The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes.

          The higher-plant shoot meristem is a dynamic structure whose maintenance depends on the coordination of two antagonistic processes, organ initiation and self-renewal of the stem cell population. In Arabidopsis shoot and floral meristems, the WUSCHEL (WUS) gene is required for stem cell identity, whereas the CLAVATA1, 2, and 3 (CLV) genes promote organ initiation. Our analysis of the interactions between these key regulators indicates that (1) the CLV genes repress WUS at the transcript level and that (2) WUS expression is sufficient to induce meristem cell identity and the expression of the stem cell marker CLV3. Our data suggest that the shoot meristem has properties of a self-regulatory system in which WUS/CLV interactions establish a feedback loop between the stem cells and the underlying organizing center.
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            The OsTB1 gene negatively regulates lateral branching in rice.

            Although the shoot apical meristem (SAM) is ultimately responsible for post-embryonic development in higher plants, lateral meristems also play an important role in determining the final morphology of the above-ground part. Axillary buds developing at the axils of leaves produce additional shoot systems, lateral branches. The rice TB1 gene (OsTB1) was first identified based on its sequence similarity with maize TEOSINTE BRANCHED 1 (TB1), which is involved in lateral branching in maize. Both genes encode putative transcription factors carrying a basic helix-loop-helix type of DNA-binding motif, named the TCP domain. The genetic locus of OsTB1 suggested that OsTB1 is a real counterpart of maize TB1. Transgenic rice plants overexpressing OsTB1 exhibited markedly reduced lateral branching without the propagation of axillary buds being affected. We also demonstrated that a rice strain carrying a classical morphological marker mutation, fine culm 1 (fc1), contain the loss-of-function mutation of OsTB1 and exhibits enhanced lateral branching. Expression of OsTB1, as examined with a putative promoter-glucuronidase (GUS) gene fusion, was observed throughout the axillary bud, as well as the basal part of the shoot apical meristem, vascular tissues in the pith and the lamina joint. Taking these data together, we concluded that OsTB1 functions as a negative regulator for lateral branching in rice, presumably through expression in axillary buds.
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              INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1.

              The domestication of cereals has involved common changes in morphological features, such as seed size, seed retention and modification of vegetative and inflorescence architecture that ultimately contributed to an increase in harvested yield. In barley, this process has resulted in two different cultivated types, two-rowed and six-rowed forms, both derived from the wild two-rowed ancestor, with archaeo-botanical evidence indicating the origin of six-rowed barley early in the domestication of the species, some 8,600-8,000 years ago. Variation at SIX-ROWED SPIKE 1 (VRS1) is sufficient to control this phenotype. However, phenotypes imposed by VRS1 alleles are modified by alleles at the INTERMEDIUM-C (INT-C) locus. Here we show that INT-C is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1 (TB1) and identify 17 coding mutations in barley TB1 correlated with lateral spikelet fertility phenotypes.
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                Author and article information

                Contributors
                smckim@dundee.ac.uk
                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                27 November 2018
                March 2019
                : 221
                : 4 ( doiID: 10.1111/nph.2019.221.issue-4 )
                : 1950-1965
                Affiliations
                [ 1 ] Cell and Molecular Sciences The James Hutton Institute Invergowrie Dundee DD2 5DA UK
                [ 2 ] Division of Plant Sciences University of Dundee at The James Hutton Institute Invergowrie Dundee DD2 5DA UK
                Author notes
                [*] [* ] Author for correspondence:

                Sarah M. McKim

                Tel: +44 (0)1382568916

                Email: smckim@ 123456dundee.ac.uk

                Article
                NPH15548 2018-27087
                10.1111/nph.15548
                6492131
                30339269
                e06eadb8-b438-44ea-be5e-ec39fc6d9fbb
                © 2018 The Authors. New Phytologist © 2018 New Phytologist Trust

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 17 May 2018
                : 22 September 2018
                Page count
                Figures: 7, Tables: 4, Pages: 16, Words: 11630
                Funding
                Funded by: Biotechnology and Biological Sciences Research Council
                Award ID: BB/K01613X/1
                Funded by: Royal Society of Edinburgh
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                cpt1265
                March 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.2.1 mode:remove_FC converted:01.05.2019

                Plant science & Botany
                barley (hordeum vulgare),branching,grain number,meristem,spikelet fertility,yield potential

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