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      Aquaporins are main contributors to root hydraulic conductivity in pearl millet [ Pennisetum glaucum (L) R. Br.]

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          Abstract

          Pearl millet is a key cereal for food security in arid and semi-arid regions but its yield is increasingly threatened by water stress. Physiological mechanisms relating to conservation of soil water or increased water use efficiency can alleviate that stress. Aquaporins (AQP) are water channels that mediate root water transport, thereby influencing plant hydraulics, transpiration and soil water conservation. However, AQP remain largely uncharacterized in pearl millet. Here, we studied AQP function in root water transport in two pearl millet lines contrasting for water use efficiency (WUE). We observed that these lines also contrasted for root hydraulic conductivity (Lpr) and AQP contribution to Lpr. The line with lower WUE showed significantly higher AQP contribution to Lpr. To investigate AQP isoforms contributing to Lpr, we developed genomic approaches to first identify the entire AQP family in pearl millet and secondly, characterize the plasma membrane intrinsic proteins (PIP) gene expression profile. We identified and annotated 33 AQP genes in pearl millet, among which ten encoded PIP isoforms. PgPIP1-3 and PgPIP1-4 were significantly more expressed in the line showing lower WUE, higher Lpr and higher AQP contribution to Lpr. Overall, our study suggests that the PIP1 AQP family are the main regulators of Lpr in pearl millet and may possibly be associated with mechanisms associated to whole plant water use. This study paves the way for further investigations on AQP functions in pearl millet hydraulics and adaptation to environmental stresses.

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          Most cited references 67

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          A silicon transporter in rice.

          Silicon is beneficial to plant growth and helps plants to overcome abiotic and biotic stresses by preventing lodging (falling over) and increasing resistance to pests and diseases, as well as other stresses. Silicon is essential for high and sustainable production of rice, but the molecular mechanism responsible for the uptake of silicon is unknown. Here we describe the Low silicon rice 1 (Lsi1) gene, which controls silicon accumulation in rice, a typical silicon-accumulating plant. This gene belongs to the aquaporin family and is constitutively expressed in the roots. Lsi1 is localized on the plasma membrane of the distal side of both exodermis and endodermis cells, where casparian strips are located. Suppression of Lsi1 expression resulted in reduced silicon uptake. Furthermore, expression of Lsi1 in Xenopus oocytes showed transport activity for silicon only. The identification of a silicon transporter provides both an insight into the silicon uptake system in plants, and a new strategy for producing crops with high resistance to multiple stresses by genetic modification of the root's silicon uptake capacity.
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            The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants.

            Major intrinsic proteins (MIPs) facilitate the passive transport of small polar molecules across membranes. MIPs constitute a very old family of proteins and different forms have been found in all kinds of living organisms, including bacteria, fungi, animals, and plants. In the genomic sequence of Arabidopsis, we have identified 35 different MIP-encoding genes. Based on sequence similarity, these 35 proteins are divided into four different subfamilies: plasma membrane intrinsic proteins, tonoplast intrinsic proteins, NOD26-like intrinsic proteins also called NOD26-like MIPs, and the recently discovered small basic intrinsic proteins. In Arabidopsis, there are 13 plasma membrane intrinsic proteins, 10 tonoplast intrinsic proteins, nine NOD26-like intrinsic proteins, and three small basic intrinsic proteins. The gene structure in general is conserved within each subfamily, although there is a tendency to lose introns. Based on phylogenetic comparisons of maize (Zea mays) and Arabidopsis MIPs (AtMIPs), it is argued that the general intron patterns in the subfamilies were formed before the split of monocotyledons and dicotyledons. Although the gene structure is unique for each subfamily, there is a common pattern in how transmembrane helices are encoded on the exons in three of the subfamilies. The nomenclature for plant MIPs varies widely between different species but also between subfamilies in the same species. Based on the phylogeny of all AtMIPs, a new and more consistent nomenclature is proposed. The complete set of AtMIPs, together with the new nomenclature, will facilitate the isolation, classification, and labeling of plant MIPs from other species.
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              Identification of 33 rice aquaporin genes and analysis of their expression and function.

              Plant aquaporins form a large protein family including plasma membrane-type (PIPs) and tonoplast-type aquaporins (TIPs), and facilitate osmotic water transport across membranes as a key physiological function. We identified 33 genes for aquaporins in the genome sequence of rice (Oryza sativa L. cv. Nipponbare). We investigated their expression levels in leaf blades, roots and anthers of rice (cv. Akitakomachi) using semi-quantitative reverse transcription-PCR (RT-PCR). At both early tillering (21 d after germination) and panicle formation (56 d) stages, six genes, including OsPIP2;4 and OsPIP2;5, were expressed predominantly in roots, while 14 genes, including OsPIP2;7 and OsTIP1;2, were found in leaf blades. Eight genes, such as OsPIP1;1 and OsTIP4;1, were evenly expressed in leaf blades, roots and anthers. Analysis by stopped-flow spectrophotometry revealed high water channel activity when OsPIP2;4 or OsPIP2;5 were expressed in yeast but not when OsPIP1;1 or OsPIP1;2 were expressed. Furthermore, the mRNA levels of OsPIP2;4 and OsPIP2;5 showed a clear diurnal fluctuation in roots; they showed a peak 3 h after the onset of light and dropped to a minimum 3 h after the onset of darkness. The mRNA levels of 10 genes including OsPIP2;4 and OsPIP2;5 markedly decreased in roots during chilling treatment and recovered after warming. The changes in mRNA levels during and after the chilling treatment were comparable with that of the bleeding sap volume. These results suggested the relationship between the root water uptake and mRNA levels of several aquaporins with high water channel activity, such as OsPIP2;4 and OsPIP2;5.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Investigation
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                1 October 2020
                2020
                : 15
                : 10
                Affiliations
                [1 ] UMR DIADE, IRD, Université de Montpellier, Montpellier, France
                [2 ] Laboratoire Mixte International Adaptation des Plantes et Microorganismes Associés Aux Stress Environnementaux, Dakar, Senegal
                [3 ] Laboratoire Commun de Microbiologie, Dakar, Senegal
                [4 ] Centre d’Étude Régional pour l’Amélioration de l’Adaptation à la Sécheresse, Thiès, Senegal
                [5 ] International Crops Research Institute for Semi-Arid Tropics (ICRISAT), Hyderabad, India
                University of Tasmania, AUSTRALIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Article
                PONE-D-20-13244
                10.1371/journal.pone.0233481
                7529256
                33001997
                © 2020 Grondin 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.

                Page count
                Figures: 5, Tables: 2, Pages: 19
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR17-CE20-0022-01
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-l0-LABX-0001-0l
                Funded by: funder-id http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-16-IDEX-0006
                This work was supported by the CGIAR Research Programme on Grain Legumes and Dryland Cereals (GLDC). PA was supported by the Cultivar program from the Agropolis Foundation as part of the "Investissement d'Avenir" (ANR-l0-LABX-0001-0l) under the frame of I-SITE MUSE (ANR-16-IDEX-0006). The French Agence Nationale de la Recherche supports the post-doctoral fellowship of CFC (ANR Grant RootAdapt n°ANR17-CE20-0022-01 to LL).
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Grasses
                Millet
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Cell Membranes
                Membrane Proteins
                Biology and Life Sciences
                Genetics
                Gene Expression
                Physical Sciences
                Chemistry
                Chemical Compounds
                Azides
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Cell Membranes
                Biology and Life Sciences
                Agriculture
                Crop Science
                Crops
                Cereal Crops
                Biology and Life Sciences
                Molecular Biology
                Macromolecular Structure Analysis
                Protein Structure
                Protein Structure Comparison
                Biology and Life Sciences
                Biochemistry
                Proteins
                Protein Structure
                Protein Structure Comparison
                Biology and Life Sciences
                Genetics
                Genomics
                Plant Genomics
                Biology and Life Sciences
                Bioengineering
                Biotechnology
                Plant Biotechnology
                Plant Genomics
                Engineering and Technology
                Bioengineering
                Biotechnology
                Plant Biotechnology
                Plant Genomics
                Biology and Life Sciences
                Plant Science
                Plant Biotechnology
                Plant Genomics
                Biology and Life Sciences
                Genetics
                Plant Genetics
                Plant Genomics
                Biology and Life Sciences
                Plant Science
                Plant Genetics
                Plant Genomics
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files. All sequences and Protein Data Bank files are available at: https://dataverse.ird.fr/dataset.xhtml?persistentId=doi:10.23708/WVCG5O. All new sequences are also available from the GenBank database (accession number MT474859 for PgPIP2-8, MT474860 for PgTIP3-1, MT474861 for PgTIP4-1, MT474862 for PgTIP4-2, MT474863 for PgTIP4-3, MT474866 for PgNIP1-2, MT474867 for PgNIP3-5, MT474868 for PgSIP1-2, MT474869 for PgSIP2-1 and MT474864 and MT474865 for TIP5-1).

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