Harnessing the potential of plant transcription factors in developing climate resilient crops to improve global food security: Current and future perspectives

Abstract

Crop plants should be resilient to climatic factors in order to feed ever-increasing populations. Plants have developed stress-responsive mechanisms by changing their metabolic pathways and switching the stress-responsive genes. The discovery of plant transcriptional factors (TFs), as key regulators of different biotic and abiotic stresses, has opened up new horizons for plant scientists. TFs perceive the signal and switch certain stress-responsive genes on and off by binding to different cis-regulatory elements. More than 50 families of plant TFs have been reported in nature. Among them, DREB, bZIP, MYB, NAC, Zinc-finger, HSF, Dof, WRKY, and NF-Y are important with respect to biotic and abiotic stresses, but the potential of many TFs in the improvement of crops is untapped. In this review, we summarize the role of different stress-responsive TFs with respect to biotic and abiotic stresses. Further, challenges and future opportunities linked with TFs for developing climate-resilient crops are also elaborated.

Keywords: Abiotic stress; Biotic stress; Climate change; Crop improvement; Food security; Plant transcription factors.

Fig. 1

Mechanism of action of transcriptional factors (TFs) for development of resistance in plants against biotic and abiotic stresses. (A) Different biotic and abiotic stresses affect plant growth and development; however, plants have developed rapid response strategies to unfavorable conditions; these involve interconnected networks at the molecular level controlled by signal cascades. The different components of stress responses are (B) signal perception, and (C) signal transduction, (D) transcriptional regulation, (E) gene expression, (F) gene adoption. When plant cells perceive a stress signal, receptors or sensors in the cell wall or membrane detect the stress stimulus, followed by a rapid response that transduces the external signal to intracellular signals. Signal cascades involving intracellular molecules or ions are activated along with kinase cascades, which are generally cytoplasmic. Major cascades are associated with reactive oxygen species (ROS) and calcium ions (Ca²⁺). Phytohormones, including abscisic acid, jasmonic acid, salicylic acid, and ethylene, are powerful second messengers that coordinate signal transduction pathways during stress responses. These signals activate several parallel transduction pathways, which often involve phosphatases and protein kinases. Following the initial step of signal perception, plants activate two major signal cascades: the mitogen-activated protein kinase (MAPK) and calcium-dependent protein kinase (CDPK) pathways. Finally, specific TFs are upregulated or downregulated by protein kinases or phosphatases, and the TFs bind to cis-elements of stress-responsive genes to enhance or suppress their transcription. Finally, stress resistant/tolerant plants emerge.

Fig. 2

Illustration of domains’ structure, composition, and cis-regulatory elements of nine TFs including WRKY, MYB, DREB, bZIP, NAC, Dof, NF-Y, HSF, and Zinc finger. WRKY: The WRKY TFs contains the N-terminal WRKYGQK domain, while at the C-terminal, Zinc Finger (ZF) motifs are present. The ZF-motif may be either Cx_4-5Cx_22-23HxH or Cx₇Cx₂₃HxC. The WRKY domain spans around 60 amino acids and is a DNA binding protein, which binds to W-BOX (TTGACT/C) and many other binding sites (Eulgem et al., 2000, Ülker and Somssich, 2004, Van Verk et al., 2008, Rushton et al., 2010, Rushton et al., 2012). MYB: The MYB domain consists of 52 amino acids repeats forming 3α-helicase, in which the second and third helicase form helix structure with three equally spaced tryptophan, forming hydrophobic core in a three-dimensional (3D) helix structure. The third helix is the “recognition helix” that directly binds to DNA and inserts it into a major grove. Two MYB repeats are bind in the major grove and recognize specific DNA target sequence during DNA contact (Dubos et al., 2010, Zhong and Ye, 2015). DREB: The DBD of DREB family members is the AP₂/ERF type with a conserved region of 60 amino acids; AP₂ family members have α-helix and β-sheet stretches at a highly conserved region, the later within the DBD. DREB proteins attach with C-repeat sequence (A/GCCGAC) or dehydration responsive elements (DRE) for activation of stress responsive genes (Fujita et al., 2005, Sharoni et al., 2011, Chen et al., 2016). bZIP: The bZIP domain is made up of a basic region at the N-terminal linked to C-terminal leucine zipper. About 16 amino acids are present in the basic region, which form an invariant motif (N-x₇-R/K) that is responsible for binding to DNA. The bZIP domain consists of two structures: N-x₇-R/K-x₉ (DNA binding site) and leucine zipper (hydrophobic amino acids, i.e., Val, Met with heptad repeats of Leu) (Liao et al., 2008, Banerjee and Roychoudhury, 2017). NAC: The NAC domain spans approximately 150 amino acids, and has five conserved sub-domains (N₁–N₅) that form motifs for protein–protein interaction, DNA binding, or TF dimerization. Structural studies have shown that DBD is located at N-terminal while regulatory domain is located at the C-terminal (Baillo et al., 2019, Yuan et al., 2019b). DoF: The Dof TFs consists of a bi-functional domain, having dual activity for DNA-binding as well as protein–protein interaction. A single ZF-is present in the C₂/C₂ domain needed for binding the target 5′-(T) AAAG-3′ sequence or its reversibly orientated sequence, CTTT, with a conserved region of target DNA sequence. The C-terminal region helps in regulation of the transcription process by interacting with different regulatory proteins. (Yanagisawa, 2002, Noguero et al., 2013). NF-Y: NF-YA has two domains with α helix structure. The N-terminal conserved region has 20 amino acids α helix A1 domain, responsible for interaction with NF-YB and NF-YC, while the C-terminal which binds with the CCAAT element has a 21 amino acid α-helix A₂ domain. NF-YB and NF-YC, is formed through the Histone Fold Domain. These domains bind with each other through head to tail. Subgroups of NF-Y are NF-YA, NF-YB, and NF-YC, binds to the CCAAT box (Petroni et al., 2012, Nardini et al., 2013, Zhao et al., 2017). HSFs: Conserved regions of HSFs include three helical structures an N-terminal DBD with four inverted β-sheets arranged in parallel fashion. The binding sites sequence termed heat responsive elements (5′-AGAAnnTTCT-3′) is recognized by the DBD hydrophobic region, which has a helix-turn-helix conformation. At the N-terminal, the oligomeric domain contains two regions of hydrophobic heptapeptide repeats HR-A and HR-B, having five and six heptapeptide repeats, respectively (Yura and Nakahigashi, 1999, Nover et al., 2001, Åkerfelt et al., 2010, Qiao et al., 2015). Zinc Finger: Most plants ZF genes have conserved QALGGH amino acid motif within the ZF domain that forms a Q-type C₂H₂ plant specific ZF subfamily. This motif is present at the N terminal on an alpha helix. The ZF-motif has zinc, along with two cysteine and two histidine molecules at base, and one alpha helix or two beta-pleated sheets arranged in anti-parallel fashion in a finger like projection. ZFs play role in sub cellular localization and stress responses (Rajavashisth et al., 1989, Iuchi, 2001, Figueiredo et al., 2012, Kaur and Subramanian, 2016).

Fig. 3

Schematic illustration of different crop improvement techniques particularly targeted modifications in TFs via gene editing/silencing for crop improvement. (A) Overview of different crop improvement techniques. (B) Different transcriptional factors that can be used for incorporation of biotic and abiotic stress tolerance in crops. (C) Different signal transduction pathways that are activated or modified by TFs. (D) Biotic and abiotic stresses that are alleviated by action of TFs.