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      Rice actin binding protein RMD controls crown root angle in response to external phosphate

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          Abstract

          Root angle has a major impact on acquisition of nutrients like phosphate that accumulate in topsoil and in many species; low phosphate induces shallower root growth as an adaptive response. Identifying genes and mechanisms controlling root angle is therefore of paramount importance to plant breeding. Here we show that the actin-binding protein Rice Morphology Determinant (RMD) controls root growth angle by linking actin filaments and gravity-sensing organelles termed statoliths. RMD is upregulated in response to low external phosphate and mutants lacking of RMD have steeper crown root growth angles that are unresponsive to phosphate levels. RMD protein localizes to the surface of statoliths, and rmd mutants exhibit faster gravitropic response owing to more rapid statoliths movement. We conclude that adaptive changes to root angle in response to external phosphate availability are RMD dependent, providing a potential target for breeders.

          Abstract

          The orientation of plant roots responds to gravity and influences nutrient acquisition. Here the authors show that the formin RMD buffers movement of specialized gravity-sensing organelles and report enhanced RMD expression during phosphate deficiency that could alter root angle to improve phosphate uptake.

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          Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions.

          The genetic improvement of drought resistance is essential for stable and adequate crop production in drought-prone areas. Here we demonstrate that alteration of root system architecture improves drought avoidance through the cloning and characterization of DEEPER ROOTING 1 (DRO1), a rice quantitative trait locus controlling root growth angle. DRO1 is negatively regulated by auxin and is involved in cell elongation in the root tip that causes asymmetric root growth and downward bending of the root in response to gravity. Higher expression of DRO1 increases the root growth angle, whereby roots grow in a more downward direction. Introducing DRO1 into a shallow-rooting rice cultivar by backcrossing enabled the resulting line to avoid drought by increasing deep rooting, which maintained high yield performance under drought conditions relative to the recipient cultivar. Our experiments suggest that control of root system architecture will contribute to drought avoidance in crops.
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            Roots of the Second Green Revolution

            The Green Revolution boosted crop yields in developing nations by introducing dwarf genotypes of wheat and rice capable of responding to fertilisation without lodging. We now need a second Green Revolution, to improve the yield of crops grown in infertile soils by farmers with little access to fertiliser, who represent the majority of third-world farmers. Just as the Green Revolution was based on crops responsive to high soil fertility, the second Green Revolution will be based on crops tolerant of low soil fertility. Substantial genetic variation in the productivity of crops in infertile soil has been known for over a century. In recent years we have developed a better understanding of the traits responsible for this variation. Root architecture is critically important by determining soil exploration and therefore nutrient acquisition. Architectural traits under genetic control include basal-root gravitropism, adventitious-root formation and lateral branching. Architectural traits that enhance topsoil foraging are important for acquisition of phosphorus from infertile soils. Genetic variation in the length and density of root hairs is important for the acquisition of immobile nutrients such as phosphorus and potassium. Genetic variation in root cortical aerenchyma formation and secondary development (‘root etiolation’) are important in reducing the metabolic costs of root growth and soil exploration. Genetic variation in rhizosphere modification through the efflux of protons, organic acids and enzymes is important for the mobilisation of nutrients such as phosphorus and transition metals, and the avoidance of aluminum toxicity. Manipulation of ion transporters may be useful for improving the acquisition of nitrate and for enhancing salt tolerance. With the noteworthy exceptions of rhizosphere modification and ion transporters, most of these traits are under complex genetic control. Genetic variation in these traits is associated with substantial yield gains in low-fertility soils, as illustrated by the case of phosphorus efficiency in bean and soybean. In breeding crops for low-fertility soils, selection for specific root traits through direct phenotypic evaluation or molecular markers is likely to be more productive than conventional field screening. Crop genotypes with greater yield in infertile soils will substantially improve the productivity and sustainability of low-input agroecosystems, and in high-input agroecosystems will reduce the environmental impacts of intensive fertilisation. Although the development of crops with reduced fertiliser requirements has been successful in the few cases it has been attempted, the global scientific effort devoted to this enterprise is small, especially considering the magnitude of the humanitarian, environmental and economic benefits being forgone. Population growth, ongoing soil degradation and increasing costs of chemical fertiliser will make the second Green Revolution a priority for plant biology in the 21st century.
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              Root system architecture: opportunities and constraints for genetic improvement of crops.

              Abiotic stresses increasingly curtail crop yield as a result of global climate change and scarcity of water and nutrients. One way to minimize the negative impact of these factors on yield is to manipulate root system architecture (RSA) towards a distribution of roots in the soil that optimizes water and nutrient uptake. It is now established that most of the genetic variation for RSA is driven by a suite of quantitative trait loci. As we discuss here, marker-assisted selection and quantitative trait loci cloning for RSA are underway, exploiting genomic resources, candidate genes and the knowledge gained from Arabidopsis, rice and other crops. Nonetheless, efficient and accurate phenotyping, modelling and collaboration with breeders remain important challenges, particularly when defining ideal RSA for different crops and target environments.
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                Author and article information

                Contributors
                malcolm.bennett@nottingham.ac.uk
                zhangdb@sjtu.edu.cn
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                11 June 2018
                11 June 2018
                2018
                : 9
                : 2346
                Affiliations
                [1 ]ISNI 0000 0004 0368 8293, GRID grid.16821.3c, Joint International Research Laboratory of Metabolic & Developmental Sciences, State Key Laboratory of Hybrid Rice, SJTU-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, , Shanghai Jiao Tong University, ; Shanghai, 200240 China
                [2 ]ISNI 0000 0004 1936 8868, GRID grid.4563.4, Centre for Plant Integrative Biology, School of Biosciences, , University of Nottingham, Loughborough Leicstershire, ; LE12 5RD Nottingham, UK
                [3 ]ISNI 0000 0001 2217 5846, GRID grid.419632.b, National Institute of Plant Genome Research (NIPGR), ; New Delhi, 110067 India
                [4 ]ISNI 0000 0004 0369 1660, GRID grid.73113.37, Department of Pharmaceutical Botany, School of Pharmacy, , Second Military Medical University, ; Shanghai, 200433 China
                [5 ]ISNI 0000 0004 1790 4137, GRID grid.35155.37, National Key Laboratory of Crop Genetic Improvement, , Huazhong Agricultural University, ; Wuhan, 430070 China
                [6 ]ISNI 0000 0001 2180 6431, GRID grid.4280.e, Department of Biological Sciences and Centre for BioImaging Sciences, , National University of Singapore, ; Singapore, 117543 Singapore
                [7 ]ISNI 0000 0004 1936 8403, GRID grid.9909.9, Centre for Plant Sciences, Faculty of Biological Sciences, , University of Leeds, ; Leeds, LS2 9JT UK
                [8 ]ISNI 0000 0004 1936 7304, GRID grid.1010.0, University of Adelaide-SJTU Joint Centre for Agriculture and Health, School of Agriculture, Food and Wine, , University of Adelaide, ; Waite Campus, Urrbrae, 5064 SA Australia
                Author information
                http://orcid.org/0000-0002-5333-8502
                http://orcid.org/0000-0002-9614-1347
                http://orcid.org/0000-0001-6969-5187
                http://orcid.org/0000-0001-5697-3707
                http://orcid.org/0000-0001-6194-6316
                http://orcid.org/0000-0003-0475-390X
                http://orcid.org/0000-0002-1764-2929
                Article
                4710
                10.1038/s41467-018-04710-x
                5995806
                29892032
                fd4c1799-586d-4fd2-bc79-18c9063ad2e9
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 23 March 2018
                : 1 May 2018
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001809, National Natural Science Foundation of China (National Science Foundation of China);
                Award ID: 3143009
                Award ID: 31322040
                Award Recipient :
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