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      Phosphorus Limitation Improved Salt Tolerance in Maize Through Tissue Mass Density Increase, Osmolytes Accumulation, and Na + Uptake Inhibition

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          Abstract

          Low phosphorus (P) availability and salt stress are two major constraints for maize ( Zea mays L.) growth in north China. A combination of salinity and high P rather than low P is more detrimental to the growth of maize. However, little is known about the mechanisms by which P nutrition modifies the salt tolerance and P uptake of maize. The present study aimed to investigate the combined effects of salinity and P on maize growth and P uptake, and to address the physiological mechanisms of salt tolerance influenced by P availability in maize. Seedlings of a local maize cultivar XY335 were grown hydroponically for 35 days under low (5 μM) or sufficient P supply (200 μM) with or without 100 mM NaCl. Root morphological traits, tissue mass density, leaf osmolytes (sugars and proline) accumulation, and Na +/K + ratio were measured to allow evaluation of the combined effects of salinity and P on maize growth and P uptake. Both P deficiency and salinity markedly reduced the growth of maize. However, P deficiency had a more pronounced effect on shoot growth while salinity affected root growth more prominently. Combined effects of P deficiency and salinity on total root length, root surface area, and average root diameter were similar to that of plants grown under salt stress. The combination of P deficiency and salinity treatments had a more pronounced effect on tissue mass density, leaf proline and soluble sugars compared to individual treatment of either low P or NaCl. When exposed to salt stress, maize plants of sufficient P accumulated greater amount of Na + than those under P deficit, but similar amounts of K + were observed between the two P treatments. Salt stress significantly increased shoot P concentration of maize with sufficient P ( P < 0.01), but not for P-deficient plants. In sum, shoots and roots of maize exhibited different responses to P deficiency and salinity, with more marked effect of P deficiency on shoots and of salinity on roots. P deficiency improved salt tolerance of maize plants, which was associated with the increase of tissue mass density, accumulation of osmolytes, reduction of Na + accumulation, and selective absorption of K + over Na +.

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          Most cited references54

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          Rapid determination of free proline for water-stress studies

          Plant and Soil, 39(1), 205-207
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            Salinity tolerance in halophytes.

            Halophytes, plants that survive to reproduce in environments where the salt concentration is around 200 mm NaCl or more, constitute about 1% of the world's flora. Some halophytes show optimal growth in saline conditions; others grow optimally in the absence of salt. However, the tolerance of all halophytes to salinity relies on controlled uptake and compartmentalization of Na+, K+ and Cl- and the synthesis of organic 'compatible' solutes, even where salt glands are operative. Although there is evidence that different species may utilize different transporters in their accumulation of Na+, in general little is known of the proteins and regulatory networks involved. Consequently, it is not yet possible to assign molecular mechanisms to apparent differences in rates of Na+ and Cl- uptake, in root-to-shoot transport (xylem loading and retrieval), or in net selectivity for K+ over Na+. At the cellular level, H+-ATPases in the plasma membrane and tonoplast, as well as the tonoplast H+-PPiase, provide the trans-membrane proton motive force used by various secondary transporters. The widespread occurrence, taxonomically, of halophytes and the general paucity of information on the molecular regulation of tolerance mechanisms persuade us that research should be concentrated on a number of 'model' species that are representative of the various mechanisms that might be involved in tolerance.
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              Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource

              Phosphorus (P) is limiting for crop yield on > 30% of the world's arable land and, by some estimates, world resources of inexpensive P may be depleted by 2050. Improvement of P acquisition and use by plants is critical for economic, humanitarian and environmental reasons. Plants have evolved a diverse array of strategies to obtain adequate P under limiting conditions, including modifications to root architecture, carbon metabolism and membrane structure, exudation of low molecular weight organic acids, protons and enzymes, and enhanced expression of the numerous genes involved in low-P adaptation. These adaptations may be less pronounced in mycorrhizal-associated plants. The formation of cluster roots under P-stress by the nonmycorrhizal species white lupin (Lupinus albus), and the accompanying biochemical changes exemplify many of the plant adaptations that enhance P acquisition and use. Physiological, biochemical, and molecular studies of white lupin and other species response to P-deficiency have identified targets that may be useful for plant improvement. Genomic approaches involving identification of expressed sequence tags (ESTs) found under low-P stress may also yield target sites for plant improvement. Interdisciplinary studies uniting plant breeding, biochemistry, soil science, and genetics under the large umbrella of genomics are prerequisite for rapid progress in improving nutrient acquisition and use in plants. Contents I. Introduction 424 II. The phosphorus conundrum 424 III. Adaptations to low P 424 IV. Uptake of P 424 V. P deficiency alters root development and function 426 VI. P deficiency modifies carbon metabolism 431 VII. Acid phosphatase 436 VIII. Genetic regulation of P responsive genes 437 IX. Improving P acquisition 439 X. Synopsis 440.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                03 July 2019
                2019
                : 10
                : 856
                Affiliations
                [1] 1College of Life Science, Hebei University , Baoding, China
                [2] 2State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University , Yangling, China
                [3] 3Institute of Soil and Water Conservation, Chinese Academy of Sciences , Yangling, China
                [4] 4UWA School of Agriculture and Environment, The Institute of Agriculture, The University of Western Australia , Perth, WA, Australia
                Author notes

                Edited by: Jose M. Garcia-Mina, University of Navarra, Spain

                Reviewed by: Petronia Carillo, Università degli Studi della Campania Luigi Vanvitelli Caserta, Italy; Fangsen Xu, Huazhong Agricultural University, China

                *Correspondence: Yinglong Chen, yinglong.chen@ 123456uwa.edu.au

                This article was submitted to Plant Nutrition, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2019.00856
                6618052
                31333699
                ac2aec9d-a3c7-44f6-b793-2fbaef54bf1a
                Copyright © 2019 Tang, Niu, Wei, Chen and Chen.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 19 February 2019
                : 14 June 2019
                Page count
                Figures: 4, Tables: 3, Equations: 3, References: 67, Pages: 10, Words: 7495
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31471946
                Award ID: 31301852
                Funded by: Natural Science Foundation of Hebei Province 10.13039/501100003787
                Award ID: C2014201138
                Funded by: Natural Science Foundation of Hebei University
                Award ID: 2014-279
                Funded by: Chinese Academy of Sciences 10.13039/501100002367
                Award ID: A315021449
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                phosphate deficiency,root growth,salt tolerance,stress physiology,osmolytes accumulation

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