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      Metabolic and molecular mechanisms underlying the foliar Zn application induced increase of 2-acetyl-1-pyrroline conferring the ‘taro-like’ aroma in pumpkin leaves

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          Abstract

          Introduction

          Fresh pumpkin leaf is popular vegetable for its rich nutrition. The pleasant taro-like odour is important aroma quality of crops, and mostly contributed by 2-acetyl-1-pyrroline in pumpkin. Element Zn can impact metabolite biosynthesis in plants, including aroma formation. However, Zn-induced biochemical responses, especially 2-acetyl-1-pyrroline formation in pumpkin, haven’t been elucidated.

          Methods

          This study integrated metabolome and transcriptome to explore molecular fluctuations in pumpkin leaves at different time intervals after foliar Zn treatment.

          Result and Discussion

          We first identified more than one thousand metabolites from pumpkin leaves by integrating different mass spectrometry methods according to the form in which a metabolite exists. Comparative metabolomic analysis revealed there were separately 25 out of 50 and 286 out of 963 metabolites that were respectively identified by gas chromatography-mass spectrometry and liquid chromatography-tandem mass spectrometry, differentially regulated by Zn treatment. Our findings revealed that 50mg/L of Zn significantly enhanced 2-acetyl-1-pyrroline production by more than 38%, which was contributed by increased biosynthesis of its precursors, including ornithine and proline. The following transcriptome analysis discovered 30,574 genes, including 953 novel genes. Zn treatment induced the differential expression of 41.6% of identified genes which were supposed to regulate the downstream metabolite changes in a time-dependent manner. Pathway analysis indicated that alternations in primary metabolism, including carbon metabolism and biosynthesis of amino acids, were vital to the fluctuated aromatic compound generation. Phytohormones and transcription factors may regulate the expression of gene P5CS and proline biosynthesis, which, therefore, affect 2-acetyl-1-pyrroline production. This research reveals molecular mechanisms of 2-acetyl-1-pyrroline formation in pumpkin, which will provide the molecular basis for desired aroma compound production through metabolite engineering.

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          Most cited references44

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          Proline: a multifunctional amino acid.

          Proline accumulates in many plant species in response to environmental stress. Although much is now known about proline metabolism, some aspects of its biological functions are still unclear. Here, we discuss the compartmentalization of proline biosynthesis, accumulation and degradation in the cytosol, chloroplast and mitochondria. We also describe the role of proline in cellular homeostasis, including redox balance and energy status. Proline can act as a signaling molecule to modulate mitochondrial functions, influence cell proliferation or cell death and trigger specific gene expression, which can be essential for plant recovery from stress. Although the regulation and function of proline accumulation are not yet completely understood, the engineering of proline metabolism could lead to new opportunities to improve plant tolerance of environmental stresses. Copyright 2009 Elsevier Ltd. All rights reserved.
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            Zinc in plants.

            Zinc (Zn) is an essential component of thousands of proteins in plants, although it is toxic in excess. In this review, the dominant fluxes of Zn in the soil-root-shoot continuum are described, including Zn inputs to soils, the plant availability of soluble Zn(2+) at the root surface, and plant uptake and accumulation of Zn. Knowledge of these fluxes can inform agronomic and genetic strategies to address the widespread problem of Zn-limited crop growth. Substantial within-species genetic variation in Zn composition is being used to alleviate human dietary Zn deficiencies through biofortification. Intriguingly, a meta-analysis of data from an extensive literature survey indicates that a small proportion of the genetic variation in shoot Zn concentration can be attributed to evolutionary processes whose effects manifest above the family level. Remarkable insights into the evolutionary potential of plants to respond to elevated soil Zn have recently been made through detailed anatomical, physiological, chemical, genetic and molecular characterizations of the brassicaceous Zn hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri.
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              Abscisic acid dynamics, signaling, and functions in plants

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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
                26 January 2023
                2023
                : 14
                : 1127032
                Affiliations
                [1] 1 Guangdong Key Laboratory for New Technology Research of Vegetables, Vegetable Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou , Guangdong, China
                [2] 2 College of Horticulture, South China Agricultural University, Guangzhou , Guangdong, China
                Author notes

                Edited by: Qiusheng Kong, Huazhong Agricultural University, China

                Reviewed by: Shuping Qu, Northeast Agricultural University, China; Jiang Shi, Tea Research Institute, Chinese Academy of Agricultural Sciences, China

                *Correspondence: Junxing Li, lijunxing@ 123456gdaas.cn

                †These authors have contributed equally to this work and share first authorship

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

                Article
                10.3389/fpls.2023.1127032
                9909474
                627fc71e-f9eb-4b8d-9a98-26075e6c1630
                Copyright © 2023 Deng, Yang, Qiu, Luo, Wu, Liu, Zhao, Gong, Zheng and Li

                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 December 2022
                : 11 January 2023
                Page count
                Figures: 6, Tables: 0, Equations: 0, References: 44, Pages: 15, Words: 8255
                Funding
                The study was funded by the Project of Basic and Applied Basic Research of Guangdong Province [2021A1515011187], Special Fund for Scientific Innovation Strategy-Construction of High Level Academy of Agriculture Science [R2022YJ-YB1001], Key-Area Research and Development Program of Guangdong Province [2020B020220003], Agricultural Competitive Industry Discipline Team Building Project of Guangdong Academy of Agricultural Sciences [202103TD], the Science and Technology Program of Guangdong Province [2020A0505020006, 2019A050520002, 2017B030314111], the Laboratory of Lingnan Modern Agriculture Project [NZ2021008], National Modern Agricultural Technology System Construction Project [CARS-23-G-50], Construction of Modern Agricultural Industry Technology System Innovation Team of Guangdong Province [2021KJ110], and the Science and Technology Program of Guangzhou of China [202102020801].
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                2-acetyl-1-pyrroline,aroma,pumpkin,metabolome,transcriptome,zn
                Plant science & Botany
                2-acetyl-1-pyrroline, aroma, pumpkin, metabolome, transcriptome, zn

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