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      Metabolic pathways engineering for drought or/and heat tolerance in cereals

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          Abstract

          Drought (D) and heat (H) are the two major abiotic stresses hindering cereal crop growth and productivity, either singly or in combination (D/+H), by imposing various negative impacts on plant physiological and biochemical processes. Consequently, this decreases overall cereal crop production and impacts global food availability and human nutrition. To achieve global food and nutrition security vis-a-vis global climate change, deployment of new strategies for enhancing crop D/+H stress tolerance and higher nutritive value in cereals is imperative. This depends on first gaining a mechanistic understanding of the mechanisms underlying D/+H stress response. Meanwhile, functional genomics has revealed several stress-related genes that have been successfully used in target-gene approach to generate stress-tolerant cultivars and sustain crop productivity over the past decades. However, the fast-changing climate, coupled with the complexity and multigenic nature of D/+H tolerance suggest that single-gene/trait targeting may not suffice in improving such traits. Hence, in this review-cum-perspective, we advance that targeted multiple-gene or metabolic pathway manipulation could represent the most effective approach for improving D/+H stress tolerance. First, we highlight the impact of D/+H stress on cereal crops, and the elaborate plant physiological and molecular responses. We then discuss how key primary metabolism- and secondary metabolism-related metabolic pathways, including carbon metabolism, starch metabolism, phenylpropanoid biosynthesis, γ-aminobutyric acid (GABA) biosynthesis, and phytohormone biosynthesis and signaling can be modified using modern molecular biotechnology approaches such as CRISPR-Cas9 system and synthetic biology (Synbio) to enhance D/+H tolerance in cereal crops. Understandably, several bottlenecks hinder metabolic pathway modification, including those related to feedback regulation, gene functional annotation, complex crosstalk between pathways, and metabolomics data and spatiotemporal gene expressions analyses. Nonetheless, recent advances in molecular biotechnology, genome-editing, single-cell metabolomics, and data annotation and analysis approaches, when integrated, offer unprecedented opportunities for pathway engineering for enhancing crop D/+H stress tolerance and improved yield. Especially, Synbio-based strategies will accelerate the development of climate resilient and nutrient-dense cereals, critical for achieving global food security and combating malnutrition.

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          Most cited references488

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          Heat tolerance in plants: An overview

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            Abiotic stress, the field environment and stress combination.

            Farmers and breeders have long known that often it is the simultaneous occurrence of several abiotic stresses, rather than a particular stress condition, that is most lethal to crops. Surprisingly, the co-occurrence of different stresses is rarely addressed by molecular biologists that study plant acclimation. Recent studies have revealed that the response of plants to a combination of two different abiotic stresses is unique and cannot be directly extrapolated from the response of plants to each of the different stresses applied individually. Tolerance to a combination of different stress conditions, particularly those that mimic the field environment, should be the focus of future research programs aimed at developing transgenic crops and plants with enhanced tolerance to naturally occurring environmental conditions.
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              Gene networks involved in drought stress response and tolerance.

              Plants respond to survive under water-deficit conditions via a series of physiological, cellular, and molecular processes culminating in stress tolerance. Many drought-inducible genes with various functions have been identified by molecular and genomic analyses in Arabidopsis, rice, and other plants, including a number of transcription factors that regulate stress-inducible gene expression. The products of stress-inducible genes function both in the initial stress response and in establishing plant stress tolerance. In this short review, recent progress resulting from analysis of gene expression during the drought-stress response in plants as well as in elucidating the functions of genes implicated in the stress response and/or stress tolerance are summarized. A description is also provided of how various genes involved in stress tolerance were applied in genetic engineering of dehydration stress tolerance in transgenic Arabidopsis 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
                22 September 2023
                2023
                : 14
                : 1111875
                Affiliations
                [1] 1Hebei Key Laboratory of Quality & Safety Analysis-Testing for Agro-Products and Food, Hebei North University , Zhangjiakou, China
                [2] 2State Key Laboratory of North China Crop Improvement and Regulation, Hebei Agricultural University , Baoding, China
                Author notes

                Edited by: Maryke T. Labuschagne, University of the Free State, South Africa

                Reviewed by: Md Atikur Rahman, Rural Development Administration, Republic of Korea; Ali Raza, Fujian Agriculture and Forestry University, China; Anuj Kumar, Dalhousie University, Canada

                *Correspondence: Zhihong Huang, hbnuhzh@ 123456163.com ; Zaimin Tian, nkxtzm@ 123456163.com
                Article
                10.3389/fpls.2023.1111875
                10557149
                37810398
                9d98c11d-4568-4a09-a152-479101205a4b
                Copyright © 2023 Liu, Zenda, Tian and Huang

                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
                : 30 November 2022
                : 04 September 2023
                Page count
                Figures: 5, Tables: 1, Equations: 0, References: 494, Pages: 32, Words: 18264
                Funding
                This research was funded by Hebei Province Science and Technology Program to Support Key Research and Development Projects (18226334D), Modern Agricultural Industrial Technology System in Hebei Province (HBCT2018020203), Youth Fund Project of Hebei Province (QN2022018), Hebei North University (XJ2023012), College Students' Innovation and Entrepreneurship Training Program Project (S202310092019), and Science and Technology Program of Hebei (21326405D).
                Categories
                Plant Science
                Review
                Custom metadata
                Plant Abiotic Stress

                Plant science & Botany
                d/+h stress,metabolic pathway,synthetic biology,pathways crosstalk,cereal crops,multiple-trait modification

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