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      Genome-Wide Identification and Characterization of Aquaporins and Their Role in the Flower Opening Processes in Carnation ( Dianthus caryophyllus)

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          Abstract

          Aquaporins (AQPs) are associated with the transport of water and other small solutes across biological membranes. Genome-wide identification and characterization will pave the way for further insights into the AQPs’ roles in the commercial carnation ( Dianthus caryophyllus). This study focuses on the analysis of AQPs in carnation (DcaAQPs) involved in flower opening processes. Thirty DcaAQPs were identified and grouped to five subfamilies: nine PIPs, 11 TIPs, six NIPs, three SIPs, and one XIP. Subsequently, gene structure, protein motifs, and co-expression network of DcaAQPs were analyzed and substrate specificity of DcaAQPs was predicted. qRT-PCR, RNA-seq, and semi-qRTRCR were used for DcaAQP genes expression analysis. The analysis results indicated that DcaAQPs were relatively conserved in gene structure and protein motifs, that DcaAQPs had significant differences in substrate specificity among different subfamilies, and that DcaAQP genes’ expressions were significantly different in roots, stems, leaves and flowers. Five DcaAQP genes ( DcaPIP1;3, DcaPIP2;2, DcaPIP2;5, DcaTIP1;4, and DcaTIP2;2) might play important roles in flower opening process. However, the roles they play are different in flower organs, namely, sepals, petals, stamens, and pistils. Overall, this study provides a theoretical basis for further functional analysis of DcaAQPs.

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          Aquaporins in Plants.

          Aquaporins are membrane channels that facilitate the transport of water and small neutral molecules across biological membranes of most living organisms. In plants, aquaporins occur as multiple isoforms reflecting a high diversity of cellular localizations, transport selectivity, and regulation properties. Plant aquaporins are localized in the plasma membrane, endoplasmic reticulum, vacuoles, plastids and, in some species, in membrane compartments interacting with symbiotic organisms. Plant aquaporins can transport various physiological substrates in addition to water. Of particular relevance for plants is the transport of dissolved gases such as carbon dioxide and ammonia or metalloids such as boron and silicon. Structure-function studies are developed to address the molecular and cellular mechanisms of plant aquaporin gating and subcellular trafficking. Phosphorylation plays a central role in these two processes. These mechanisms allow aquaporin regulation in response to signaling intermediates such as cytosolic pH and calcium, and reactive oxygen species. Combined genetic and physiological approaches are now integrating this knowledge, showing that aquaporins play key roles in hydraulic regulation in roots and leaves, during drought but also in response to stimuli as diverse as flooding, nutrient availability, temperature, or light. A general hydraulic control of plant tissue expansion by aquaporins is emerging, and their role in key developmental processes (seed germination, emergence of lateral roots) has been established. Plants with genetically altered aquaporin functions are now tested for their ability to improve plant tolerance to stresses. In conclusion, research on aquaporins delineates ever expanding fields in plant integrative biology thereby establishing their crucial role in plants.
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            The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions.

            Aquaporins, found in virtually all living organisms, are membrane-intrinsic proteins that form water-permeable complexes. The mammalian aquaporin AQP1 has also shown CO2 permeability when expressed heterologously in Xenopus oocytes, although whether this is a biochemical curiosity or of physiological significance is a matter of debate. Here we report that, in the same expression system, a CO2 permeability comparable to that of the human AQP1 is observed for the tobacco plasma membrane aquaporin NtAQP1. NtAQP1 facilitates CO2 membrane transport in the homologous plant system at the cellular level, and has a significant function in photosynthesis and in stomatal opening. NtAQP1 overexpression heightens membrane permeability for CO2 and water, and increases leaf growth. The results indicate that NtAQP1-related CO2 permeability is of physiological importance under conditions where the CO2 gradient across a membrane is small, as is the case between the atmosphere and the inside of a plant cell.
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              Unexpected complexity of the Aquaporin gene family in the moss Physcomitrella patens

              Background Aquaporins, also called major intrinsic proteins (MIPs), constitute an ancient superfamily of channel proteins that facilitate the transport of water and small solutes across cell membranes. MIPs are found in almost all living organisms and are particularly abundant in plants where they form a divergent group of proteins able to transport a wide selection of substrates. Results Analyses of the whole genome of Physcomitrella patens resulted in the identification of 23 MIPs, belonging to seven different subfamilies, of which only five have been previously described. Of the newly discovered subfamilies one was only identified in P. patens (Hybrid Intrinsic Protein, HIP) whereas the other was found to be present in a wide variety of dicotyledonous plants and forms a major previously unrecognized MIP subfamily (X Intrinsic Proteins, XIPs). Surprisingly also some specific groups within subfamilies present in Arabidopsis thaliana and Zea mays could be identified in P. patens. Conclusion Our results suggest an early diversification of MIPs resulting in a large number of subfamilies already in primitive terrestrial plants. During the evolution of higher plants some of these subfamilies were subsequently lost while the remaining subfamilies expanded and in some cases diversified, resulting in the formation of more specialized groups within these subfamilies.
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                Author and article information

                Journal
                Molecules
                Molecules
                molecules
                Molecules : A Journal of Synthetic Chemistry and Natural Product Chemistry
                MDPI
                1420-3049
                29 July 2018
                August 2018
                : 23
                : 8
                : 1895
                Affiliations
                [1 ]Key Laboratory of Horticultural Plant Biology, Ministry of Education, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, China; Asuraprince@ 123456126.com (W.K.); mohammed.bendahmane@ 123456ens-lyon.fr (M.B.)
                [2 ]Key Laboratory of Urban Agriculture in Central China (pilot run), Ministry of Agriculture, Wuhan 430070, China
                [3 ]State Key Laboratory for Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan 430072, China
                [4 ]Laboratoire Reproduction et Development des Plantes, Ecole Normale Supérieure Lyon, 520074 Lyon, France
                Author notes
                [* ]Correspondence: fuxiaopeng@ 123456mail.hzau.edu.cn ; Tel.: +86-159-2625-8658; Fax: +86-027-8728-2010
                Author information
                https://orcid.org/0000-0003-1661-1060
                Article
                molecules-23-01895
                10.3390/molecules23081895
                6222698
                30060619
                c3a26880-f781-47ec-89a3-3dbe4e38865d
                © 2018 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 05 July 2018
                : 25 July 2018
                Categories
                Article

                aqp,carnation,qrt-pcr,rna-seq,co-expression network,flower opening process

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