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Plant Secondary Metabolite Biosynthesis and Transcriptional Regulation in Response to Biotic and Abiotic Stress Conditions

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Plant Secondary Metabolite Biosynthesis and Transcriptional Regulation in Response to Biotic and Abiotic Stress Conditions agronomy Review Plant Secondary Metabolite Biosynthesis and Transcriptional Regulation in Response to Biotic and Abiotic Stress Conditions Rahmatullah Jan 1,2,† , Sajjad Asaf 3,† , Muhammad Numan 4, Lubna 5 and Kyung-Min Kim 1,2,* 1 Division of Plant Biosciences, School of Applied Biosciences, College of Agriculture & Life Science, Kyungpook National University, Daegu 41566, Korea; [email protected] 2 Costal Agriculture Research Institute, Kyungpook National University, Daegu 41566, Korea 3 Natural and Medical Science Research Center, University of Nizwa, Nizwa 616, Oman; [email protected] 4 Laboratory of Molecular Biology and Biotechnology, Department of Biology, University of North Carolina at Greensboro, Greensboro, NC 27412, USA; [email protected] 5 Department of Botany, Garden Campus, Abdul Wali Khan University, Mardan 23200, Pakistan; [email protected] * Correspondence: [email protected] † These authors contribute equally to this manuscript. Abstract: Plant secondary metabolites (SMs) play important roles in plant survival and in creating ecological connections between other species. In addition to providing a variety of valuable natural products, secondary metabolites help protect plants against pathogenic attacks and environmental stresses. Given their sessile nature, plants must protect themselves from such situations through ac- cumulation of these bioactive compounds. Indeed, secondary metabolites act as herbivore deterrents, barriers against pathogen invasion, and mitigators of oxidative stress. The accumulation of SMs Citation: Jan, R.; Asaf, S.; Numan, are highly dependent on environmental factors such as light, temperature, soil water, soil fertility, M.; Lubna; Kim, K.-M. Plant and salinity. For most plants, a change in an individual environmental factor can alter the content Secondary Metabolite Biosynthesis of secondary metabolites even if other factors remain constant. In this review, we focus on how and Transcriptional Regulation in individual environmental factors affect the accumulation of secondary metabolites in plants during Response to Biotic and Abiotic Stress both biotic and abiotic stress conditions. Furthermore, we discuss the application of abiotic and Conditions. Agronomy 2021, 11, 968. biotic elicitors in culture systems as well as their stimulating effects on the accumulation of secondary https://doi.org/10.3390/ metabolites. Specifically, we discuss the shikimate pathway and the aromatic amino acids produced agronomy11050968 in this pathway, which are the precursors of a range of secondary metabolites including terpenoids, alkaloids, and sulfur- and nitrogen-containing compounds. We also detail how the biosynthesis Academic Editor: Pilar Soengas of important metabolites is altered by several genes related to secondary metabolite biosynthesis Received: 19 April 2021 pathways. Genes responsible for secondary metabolite biosynthesis in various plant species during Accepted: 11 May 2021 stress conditions are regulated by transcriptional factors such as WRKY, MYB, AP2/ERF, bZIP, bHLH, Published: 13 May 2021 and NAC, which are also discussed here. Publisher’s Note: MDPI stays neutral Keywords: alkaloids; bioactive; deterrent; herbivores; salinity; terpenoids with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction Compounds produced by plants are categorized into primary and secondary metabo- lites (SMs). Primary metabolites, such as carbohydrates, lipids, and proteins, are directly Copyright: © 2021 by the authors. involved in plant development and growth. In contrast, SMs are multifunctional metabo- Licensee MDPI, Basel, Switzerland. lites that are typically involved in plant defense and environmental communication [1]. This article is an open access article Furthermore, they are associated with plant color, taste, and scent. Critically, they are distributed under the terms and also involved in the responses of plants to stress. For example, SMs are involved in the conditions of the Creative Commons termination of infection, whether biotic- or abiotic-related [2]. Along with their importance Attribution (CC BY) license (https:// in biotic stress tolerance, plant SMs are also involved in mitigating abiotic stresses such as creativecommons.org/licenses/by/ temperature, drought, salinity, and UV light stresses [3]. When faced with certain biotic 4.0/). Agronomy 2021, 11, 968. https://doi.org/10.3390/agronomy11050968 https://www.mdpi.com/journal/agronomy Agronomy 2021, 11, 968 2 of 31 Agronomy 2021, 11, x FOR PEER REVIEW 2 of 31 and abiotic stresses, plants can reduce morphological traits such as the number of leaves or branches, leaf area, height, and root volume [4].]. Indeed, plants have a diverse array of defense mechanisms that a allowllow them to cope with stress stress conditions, mitigate abiotic stress at the metabolomic level, and enhance SM accumulation during stress.Threat signals are at the metabolomic level, and enhance SM accumulation during stress.Threat signals are recognized by plants’ receptors and sensors, which enable defensive responses in order to recognized by plants’ receptors and sensors, which enable defensive responses in order to protect them from these stresses. The accumulation of secondary metabolites is one of the protect them from these stresses. The accumulation of secondary metabolites is one of the responses (Figure1).Transcriptional factors (TFs) play a role in plant defense control by responses (Figure 1).Transcriptional factors (TFs) play a role in plant defense control by detecting stress signals and directing downstream defense gene expression. Similarly, the detecting stress signals and directing downstream defense gene expression. Similarly, the plant’s survival, durability, and productivity are all dependent on increased synthesis of plant’s survival, durability, and productivity are all dependent on increased synthesis of secondary metabolites, known as elicitation. Various biotic (fungi, bacteria, etc.) and abiotic secondary metabolites, known as elicitation. Various biotic (fungi, bacteria, etc.) and abi- (exogenous hormones) elicitors are used to enhance secondary metabolites production in otic (exogenous hormones) elicitors are used to enhance secondary metabolites produc- plants to protect them from stress stimuli (Figure1). tion in plants to protect them from stress stimuli (Figure 1). Figure 1. Diverse biotic and abiotic stresses affect plant growth and development; plants adopt various strategies and Figure 1. Diverse biotic and abiotic stresses affect plant growth and development; plants adopt various strategies and defense defense mechanisms to mitigate these stresses. To illustrate the modulation of secondary metabolism by various transcrip- tionmechanisms factors, which to mitigate are regulated these stresses. by complicated To illustrate upstream the modulation signaling ofsecondary pathways metabolismin response byto variousstress, four transcription plant secondary factors, whichmetabolite are regulatedtypes involved by complicated in various upstreammodes of signalingresistance pathwaysare exemplified. in response to stress, four plant secondary metabolite types involved in various modes of resistance are exemplified. Plants produce SMs through several metabolic pathways that effectively respond to stressPlants conditions. produce These SMs pathways through severalare initiated metabolic from primary pathways metabolite that effectively pathways, respond which to stress conditions. These pathways are initiated from primary metabolite pathways, which produce the ultimate precursors of SMs. The shikimate pathway is the initial pathway for produce the ultimate precursors of SMs. The shikimate pathway is the initial pathway for biosynthesis of aromatic amino acids; it is activated in stress conditions to produced tryp- biosynthesis of aromatic amino acids; it is activated in stress conditions to produced trypto- tophan, tyrosine, and phenylalanine, which further enhance SM biosynthesis [5]. Different phan, tyrosine, and phenylalanine, which further enhance SM biosynthesis [5]. Different SMs accumulate conditionally in various plant parts depending on the stress condition. SMs accumulate conditionally in various plant parts depending on the stress condition. For example, phytoalexins have antimicrobial activities against phytopathogens and ac- For example, phytoalexins have antimicrobial activities against phytopathogens and accu- cumulate at high levels in leaves [6]. In addition to their antimicrobial properties, some SMs mulate at high levels in leaves [6]. In addition to their antimicrobial properties, some SMs participate in the construction of polymeric barriers to pathogen penetration. In this regard, participate in the construction of polymeric barriers to pathogen penetration. In this regard, plants have a sophisticated recognition and signaling system that enables rapid recognition plants have a sophisticated recognition and signaling system that enables rapid recogni- of pathogen attack and can initiate a dynamic defensive response. Accumulation of SMs in tion of pathogen attack and can initiate a dynamic defensive response. Accumulation of response to stress conditions is regulated at the molecular level by various genes and tran- scription factors (TFs) including those of the phytohormonal pathway (Figure 1). Among all Agronomy 2021, 11, 968 3 of 31 Agronomy 2021, 11, x FOR PEER REVIEW 3 of 31 SMs in response to stress conditions is regulated at the molecular level
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