Overexpression of SlMBP22 in Tomato Affects Plant Growth and Enhances Tolerance to Drought Stress
Introduction
MADS-box domain proteins are one of the largest families of plant transcription factors (TFs), and they play prominent roles in multiple aspects of plant development [1,2]. Based on their evolutionary origin, these proteins have been classified into two main lineages, namely, type I and type II [3]. Type I MADS-box genes can be further divided into three subfamilies: Mα, Mβ and Mγ [4]. Knowledge of type I MADS-domain proteins is limited and their regulatory roles remain to be discovered [5]. By contrast, several type II proteins have been reported as major genes that participate in eudicot and monocot crops domestication to meet specific breeding goals [6]. The plant-specific type II MADS-box factors possess a stereotypical MIKC structure, that is composed of the MADS (M), I, K and C-terminal domains [7]. Based on their phylogenetic relationships and domain structure characteristics, MIKC-type proteins have been further subdivided into the MIKCC and MIKC* groups. Furthermore, MIKCC type factors have been grouped into at least 13 distinctive subfamilies based on their phylogeny, and their functions have been reported in more detail [4,6,8,9].
In the beginning, MADS proteins were identified as major regulators of floral organ identity. The first MADS-box genes identified, AGAMOUS (AG) and DEFICIENS (DEF) from Arabidopsis thaliana [10] and Antirrhinum majus [11], respectively, were reported to participate in the regulation of floral organs almost three decades ago. With the further analysis of floral organ identity determination, MADS-box genes were subdivided into A, B, C, D and E classes [12,13]. Recently, genetic and molecular analyses revealed that MADS-domain proteins play essential roles in the morphogenesis of almost all tissues and organs and are important throughout the plant life cycle, such as in determining meristem identity [14], controlling the flowering time [15], floral organ development, senescence and abscission [[16], [17], [18], [19], [20]], inflorescence determinacy and architecture control [[21], [22], [23]], plant root and leaf growth [[24], [25], [26], [27]], fruit development and ripening [[28], [29], [30], [31]], embryo and seed development [5,[32], [33], [34], [35]], and the formation of the dehiscence zone [36]. An Arabidopsis Bs-group MADS-box gene, GORDITA (GOA), controls fruit size by restraining cell expansion [30]. ABS (TT16), a close paralog of GOA, controls inner integument differentiation and seed maturation [32,34,35]. FLORAL BINDING PROTEIN 24 (FBP24) in petunia has similar developmental roles as TT16 [32]. The wheat MADS-box gene VRN1 is critical in the regulation of plant height, spikelet development, flowering time control, as well as in the differentiation of floral meristem [37,38]. Two C-class genes, OSMADS3 and OSMADS58, have predominant functions in distinct rice floral whorls [39]. Overexpression of SlFYFL can delay senescence and abscission [40]. In tomato, SlMBP11 and SlMBP15 participate in the regulation of both vegetative and reproductive growth [41,42]. Tomato is the model species for research in fleshy fruit development and ripening [4]. The tomato MADS-box transcription factor RIPENING INHIBITOR (RIN) has been regarded as a key regulator of fruit ripening [43]. Dual suppression of FUL1 and FUL2 delays fruit ripening by inhibiting ethylene biosynthesis and reducing carotenoid content [44]. Previous research revealed that functions of many MADS-box genes are conserved among and in other flowering plants [[45], [46], [47], [48]].
Abiotic stress conditions seriously affect developmental processes and productivity, such as salinity, drought and extreme temperature. When plants encounter adverse growth conditions, a diversity of responses are induced by complex regulatory networks to cope with particular stress environments and to improve their performance. Notably, plant stress-associated transcription factors can elicit multiple biochemical and developmental pathways and play a pivotal role in rapid and fine-tuned regulation in the context of regulatory networks [[49], [50], [51]]. Early studies have shown that several transcription factor families, primarily focusing on AP2/EREBP, ERF, NAC, WRKY and MYB, are involved in plant stress or defence responses [52,53]. In addition to the functions of MADS-box proteins in different aspects of plant growth and development, further in-depth studies have suggested that some MADS-box proteins regulate the tolerance of abiotic stresses in Arabidopsis [54], wheat [55], rice [56] and tomato [57,58]. For example, in Arabidopsis, the ice1 mutation affects the transcript levels of many cold-responsive genes [54], and AGL21 overexpression lines become hypersensitive to salt stress [59]. Identification and characterization of the wheat MADS-box transcript factor family showed that many genes were affected during abiotic and biotic stress conditions [55]. In rice, OsMADS57 acts as an important regulator in optimizing chilling stress resistance [60]. Additionally, OsMADS26, OsMADS22 and OsMADS55 have been found to be involved in stress tolerance [56,61]. Tomato (Solanum lycopersicum), an economically important vegetable crop grown worldwide, is susceptible to a variety of seasonal fluctuations and environmental stress conditions. Previous studies indicated that the expression levels of tomato MADS-box genes including TM4, TM5, TM6 and TAG1, were dramatically altered, which could be connected with flower abnormalities under low temperature stress [62]. A recent study found that the MADS-box gene SlMBP11 can be significantly induced under NaCl, dehydration and wounding treatments. Moreover, suppression of SlMBP11 reduced salt stress resistance and altered several corresponding parameters, including reducing chlorophyll and relative water content and increasing the MDA level and relative electrolyte leakage in tomato plants. In contrast, SlMBP11 overexpression plants exhibited improved tolerance to salt stress compared to non-transgenic plants [57]. Downregulation of SIMBP8 enhanced resistance to drought and salt stress in tomato [58]. However, despite some emerging research, little is known about the stress resistance-related functions of the MADS-box family genes in tomato.
In this study, we isolated a MADS-box gene SlMBP22. Our data revealed that SlMBP22, participates in the regulation of auxin and GA homeostasis, in the effects of multiple phenotypes in terms of dwarf, restricted leaf expansion and darker green leaves, and tolerance of drought stress, suggesting that it might play a regulatory role in balancing plant growth and development processes, and in stress response in tomato.
Section snippets
Plant materials and growth conditions
All plants including wild-type (WT) tomato (Solanum lycopersicum AC)and transgenic seedlings were grown in a greenhouse under standard conditions (16-h-day/8-h-night cycle, 25 °C/18 °C day/night temperature, 80% humidity, and 250 μmol m -2 s -1 light intensity). The transgenic tomato plants used in our experiment from the first generation (T0) and the third generation (T2) came from tissue culture and seedlings, respectively.
To detect the expression pattern of SlMBP22, flowers were tagged at
Sequence and phylogenetic tree analyses of SlMBP22
MADS-box transcription factors govern numerous developmental processes in flowering plants. To investigate the potential roles of Bsister (Bs) MADS-box proteins in tomato, we isolated and cloned a MADS-box gene from AC++ based on the sequence available in GenBank with accession number XP_019066630.1, named SlMBP22 according to our previous report [71]. The cDNA of SlMBP22 contains an ORF of 717 bp, which encodes a protein of 238 amino acid residues.
Alignments of SlMBP22 with other typical
Discussion
MADS-domain proteins constitute one of the best-studied transcription factor families in plants. They play a prominent role in plant developmental processes. Recent studies suggested that MADS-box factors participate in plant stress responses [[54], [55], [56], [57], [58]]. The Bsister (Bs) MADS-box genes have been identified in a few flowering plants and gymnosperms and are closely related to the B class floral homeotic proteins. It has been suggested that Bs genes as key regulators are
Authors contributions
Z.H., and G.C. designed research; F.L., X.C., S.Z., Q.X., Y.W., and X.X. performed the experiments; F.L. wrote the paper. All authors have read and approved the final version of the manuscript.
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgments
This work was supported by the National Natural Science Foundation of China (nos. 31872121, 31801870), and the Natural Science Foundation of Chongqing of China (cstc2018jcyjAX0458).
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2022, International Journal of Biological MacromoleculesCitation Excerpt :HvMADS1 is responsible for maintaining the unbranched spike architecture of barley at high temperatures [28]. In tomato, MADS-box genes TM4, TM5, TM6, and TAG1can be induced by low temperatures [16], and overexpression of SlMBP22 enhances tolerance to drought stress [29]. In addition, overexpression of SlMBP11 enhances salt stress resistance by reducing relative electrolyte leakage and malondialdehyde content [30].
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2022, Journal of Plant PhysiologyCitation Excerpt :The TT16/ABS gene has been identified as a member of the Bsister subfamily of MADS-domain proteins, which is well described in A. thaliana (Kaufmann et al., 2005; Mizzotti et al., 2012; Nesi et al., 2002; Xu et al., 2017), P. hybrida (de Folter et al., 2006; Tonaco et al., 2006), and B. napus (Chen et al., 2013; Deng et al., 2012). More recently, we identified a tomato Bs gene SlMBP22, homologous to Arabidopsis ABS/TT16 and petunia FBP24, that participates in regulating tomato vegetative development and drought stress responses (Li et al., 2020). However, reports on the functional characteristics of SlMBP22 in tomato reproductive development are limited.
Jasmonate signaling restricts root soluble sugar accumulation and drives root-fungus symbiosis loss at flowering by antagonizing gibberellin biosynthesis
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These authors have contributed equally to this work.