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      Identification of key gene networks controlling polysaccharide accumulation in different tissues of Polygonatum cyrtonema Hua by integrating metabolic phenotypes and gene expression profiles

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          Abstract

          Plant polysaccharides, a type of important bioactive compound, are involved in multiple plant defense mechanisms, and in particular polysaccharide-alleviated abiotic stress has been well studied. Polygonatum cyrtonema Hua ( P. cyrtonema Hua) is a medicinal and edible perennial plant that is used in traditional Chinese medicine and is rich in polysaccharides. Previous studies suggested that sucrose might act as a precursor for polysaccharide biosynthesis. However, the role of sucrose metabolism and transport in mediating polysaccharide biosynthesis remains largely unknown in P. cyrtonema Hua. In this study, we investigated the contents of polysaccharides, sucrose, glucose, and fructose in the rhizome, stem, leaf, and flower tissues of P. cyrtonema Hua, and systemically identified the genes associated with the sucrose metabolism and transport and polysaccharide biosynthesis pathways. Our results showed that polysaccharides were mainly accumulated in rhizomes, leaves, and flowers. Besides, there was a positive correlation between sucrose and polysaccharide content, and a negative correlation between glucose and polysaccharide content in rhizome, stem, leaf, and flower tissues. Then, the transcriptomic analyses of different tissues were performed, and differentially expressed genes related to sucrose metabolism and transport, polysaccharide biosynthesis, and transcription factors were identified. The analyses of the gene expression patterns provided novel regulatory networks for the molecular basis of high accumulation of polysaccharides, especially in the rhizome tissue. Furthermore, our findings explored that polysaccharide accumulation was highly correlated with the expression levels of SUS, INV, SWEET, and PLST, which are mediated by bHLH, bZIP, ERF, ARF, C2H2, and other genes in different tissues of P. cyrtonema Hua. Herein, this study contributes to a comprehensive understanding of the transcriptional regulation of polysaccharide accumulation and provides information regarding valuable genes involved in the tolerance to abiotic stresses in P. cyrtonema Hua.

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          Most cited references60

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          Sugar transporters for intercellular exchange and nutrition of pathogens.

          Sugar efflux transporters are essential for the maintenance of animal blood glucose levels, plant nectar production, and plant seed and pollen development. Despite broad biological importance, the identity of sugar efflux transporters has remained elusive. Using optical glucose sensors, we identified a new class of sugar transporters, named SWEETs, and show that at least six out of seventeen Arabidopsis, two out of over twenty rice and two out of seven homologues in Caenorhabditis elegans, and the single copy human protein, mediate glucose transport. Arabidopsis SWEET8 is essential for pollen viability, and the rice homologues SWEET11 and SWEET14 are specifically exploited by bacterial pathogens for virulence by means of direct binding of a bacterial effector to the SWEET promoter. Bacterial symbionts and fungal and bacterial pathogens induce the expression of different SWEET genes, indicating that the sugar efflux function of SWEET transporters is probably targeted by pathogens and symbionts for nutritional gain. The metazoan homologues may be involved in sugar efflux from intestinal, liver, epididymis and mammary cells.
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            Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development.

            Karen Koch (2004)
            Sucrose cleavage is vital to multicellular plants, not only for the allocation of crucial carbon resources but also for the initiation of hexose-based sugar signals in importing structures. Only the invertase and reversible sucrose synthase reactions catalyze known paths of sucrose breakdown in vivo. The regulation of these reactions and its consequences has therefore become a central issue in plant carbon metabolism. Primary mechanisms for this regulation involve the capacity of invertases to alter sugar signals by producing glucose rather than UDPglucose, and thus also two-fold more hexoses than are produced by sucrose synthase. In addition, vacuolar sites of cleavage by invertases could allow temporal control via compartmentalization. In addition, members of the gene families encoding either invertases or sucrose synthases respond at transcriptional and posttranscriptional levels to diverse environmental signals, including endogenous changes that reflect their own action (e.g. hexoses and hexose-responsive hormone systems such as abscisic acid [ABA] signaling). At the enzyme level, sucrose synthases can be regulated by rapid changes in sub-cellular localization, phosphorylation, and carefully modulated protein turnover. In addition to transcriptional control, invertase action can also be regulated at the enzyme level by highly localized inhibitor proteins and by a system that has the potential to initiate and terminate invertase activity in vacuoles. The extent, path, and site of sucrose metabolism are thus highly responsive to both internal and external environmental signals and can, in turn, dramatically alter development and stress acclimation.
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              Sucrose efflux mediated by SWEET proteins as a key step for phloem transport.

              Plants transport fixed carbon predominantly as sucrose, which is produced in mesophyll cells and imported into phloem cells for translocation throughout the plant. It is not known how sucrose migrates from sites of synthesis in the mesophyll to the phloem, or which cells mediate efflux into the apoplasm as a prerequisite for phloem loading by the SUT sucrose-H(+) (proton) cotransporters. Using optical sucrose sensors, we identified a subfamily of SWEET sucrose efflux transporters. AtSWEET11 and 12 localize to the plasma membrane of the phloem. Mutant plants carrying insertions in AtSWEET11 and 12 are defective in phloem loading, thus revealing a two-step mechanism of SWEET-mediated export from parenchyma cells feeding H(+)-coupled import into the sieve element-companion cell complex. We discuss how restriction of intercellular transport to the interface of adjacent phloem cells may be an effective mechanism to limit the availability of photosynthetic carbon in the leaf apoplasm in order to prevent pathogen infections.
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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
                29 September 2022
                2022
                : 13
                : 1012231
                Affiliations
                [1] 1Anhui Engineering Laboratory for Agro-Products Processing, School of Tea & Food Science and Technology, Anhui Agricultural University , Hefei, China
                [2] 2Anhui Promotion Center for Technology Achievements Transfer, Anhui Academy of Science and Technology , Hefei, China
                [3] 3Jinzhai Senfeng Agricultural Technology Development Co., Ltd. , Lu’an, China
                Author notes

                Edited by: Weicong Qi, Jiangsu Academy of Agricultural Sciences (JAAS), China

                Reviewed by: Zhaojun Wei, Hefei University of Technology, China; Xiangpeng Leng, Qingdao Agricultural University, China

                *Correspondence: Ziping Chen, zpchen@ 123456ahau.edu.cn

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

                Article
                10.3389/fpls.2022.1012231
                9558278
                36247596
                2a763515-fc74-48ce-8a7b-bc552f6e997b
                Copyright © 2022 Chen, Xu, Liu, Zu, Zhang, Du, Chen, Li, Wang, Wang, Chen, Chen and Du.

                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
                : 05 August 2022
                : 29 August 2022
                Page count
                Figures: 11, Tables: 0, Equations: 0, References: 60, Pages: 17, Words: 8617
                Funding
                Funded by: Anhui Provincial Key Research and Development Plan , doi 10.13039/501100017668;
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                polysaccharides,sucrose metabolism and transport,transcription factors,gene expression,polygonatum cyrtonema hua

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