Faujiah Nurhasanah Ritonga
Yiran Xu
Bing Cui
Xingfu Liu1,3- 1Shandong Key Laboratory of Bulk Open-field Vegetable Breeding, Ministry of Agriculture and Rural Affairs Key Laboratory of Huang Huai Protected Horticulture Engineering, Institute of Vegetables, Shandong Academy of Agricultural Sciences, Jinan, China
- 2Faculty of Forestry, Universitas Sumatera Utara, Medan, Indonesia
- 3College of Horticulture Science and Engineering, Shandong Agricultural University, Taian, China
SQUAMOSA Promoter-Binding Protein-Like (SPL) transcription factors are a plant-specific family of regulatory proteins defined by a conserved SBP DNA-binding domain. They play essential roles in plant growth and development, coordinating processes such as the transition from juvenile to adult phase, branching, flowering time, and organ morphogenesis. SPL activity is tightly regulated by the miR156/157 pathway, forming a critical developmental module that integrates intrinsic and environmental cues. Recent research has expanded their known functions beyond development, revealing that SPLs also contribute to plant responses to abiotic stresses such as drought, salinity, nutrient deficiency, and temperature extremes, as well as biotic stresses including pathogen attack. Functional genomics studies across diverse species, including Arabidopsis, rice, maize, and forest trees, have uncovered both conserved and species-specific roles, emphasizing SPLs as key regulatory hubs in plant adaptation and productivity. This review summarizes advances in understanding SPL gene evolution, regulatory mechanisms, and interaction networks, with a focus on their relevance to plant architecture, leaf development, stress tolerance and crop improvement. Future applications of SPL research, particularly through gene editing, molecular breeding, and biotechnological innovations, present opportunities to optimize plant architecture, enhance resilience, and support sustainable agriculture and forestry in the face of climate change.
1 Introduction
Plant growth and development are governed by complex regulatory networks, with transcription factors (TFs) functioning as key modulators of gene expression in response to both intrinsic developmental cues and environmental conditions (Khoso et al., 2022). Acting as molecular switches, TFs influence a wide range of physiological processes including meristem activity, organ initiation, phase transitions, and responses to abiotic stress (Huang et al., 2021; Chopy et al., 2023; John et al., 2024). Their regulatory versatility makes them central to the coordination of plant form, adaptability, and productivity (Ritonga et al., 2021).
Among these TFs, the SQUAMOSA Promoter-Binding Protein-Like (SPL) family constitutes a lineage-specific group unique to the plant kingdom (Chen et al., 2010). SPL proteins possess a conserved SQUAMOSA Promoter-Binding Protein (SBP) domain that interacts with GTAC motifs in the promoters of target genes (Zhang et al., 2022). First identified in Antirrhinum majus and later in Arabidopsis thaliana, SPLs have been studied in diverse species, including Oryza sativa, A. thaliana, and Triticum aestivum (Xie et al., 2006; Wang et al., 2009; Li et al., 2022). These TFs are best known for regulating developmental phase transitions, flowering time, branching, and organ morphogenesis (Chen et al., 2010). Their expression is post-transcriptionally repressed by microRNAs, particularly miR156 and its paralog miR157, a mechanism that confers age-dependent control over SPL activity (Wang and Wang, 2015; Zhu et al., 2022). Functional studies have revealed that certain SPLs, such as SPL2, SPL5, and SPL16, exhibit partially redundant but distinct roles in shaping plant architecture through temporal and tissue-specific expression patterns (Cao et al., 2019; Sun et al., 2024; Zhang et al., 2024).
Leaf development represents a key facet of plant morphogenesis, determining photosynthetic capacity, plant architecture, and stress resilience. Traits such as leaf shape, curvature, angle, and size influence light interception, gas exchange, and developmental timing, and are therefore of agronomic importance (Ritonga et al., 2023; Nikolopoulos et al., 2024). Recent research has uncovered that SPLs function at multiple levels of leaf development, influencing processes such as juvenile-to-adult phase transitions, adaxial–abaxial polarity, and leaf blade curvature (Wang et al., 2021; Li et al., 2025a). For instance, HB34 regulate plant architecture in Arabidopsis by forming a regulatory module with miR157 and SPL10. HB34 directly represses miR157 and activates AtSPL10, establishing a feed-forward loop that influences branching and inflorescence structure in Arabidopsis leaves (Lee et al., 2022), while SPL9 contributes to freezing tolerance in A. thaliana by directly controlling the expression of the AtCBF2 gene (Zhao et al., 2022b). Additionally, SPLs integrate hormonal signals such as cytokinin, gibberellin, and auxin, modulating growth plasticity under varying environmental conditions (Song et al., 2020).
In this review, we aim to integrate current knowledge of how SPL TFs regulate leaf development across plant species. We examine their molecular interactions with genetic and hormonal pathways, their roles in developmental transitions and morphogenesis, and their responses to environmental cues. We also discuss the potential applications of SPLs in crop improvement, particularly in optimizing leaf traits for enhanced light capture, improved canopy architecture, and increased stress tolerance. By linking fundamental discoveries from model systems with translational insights from crop research, we highlight the multifaceted role of SPLs in shaping plant form and performance.
2 Overview of SPL transcription factors
The SQUAMOSA Promoter-Binding Protein-Like (SPL) transcription factors constitute a plant-specific gene family initially discovered in A. majus due to their capacity to bind the promoter of the floral meristem identity gene SQUAMOSA (Preston and Hileman, 2010). Since their discovery, SPL genes have been characterized in various plant species, where they regulate a wide range of developmental processes, including phase transitions, flowering, organ morphogenesis, and responses to environmental cues (Chen et al., 2010; Song et al., 2020; Zhu et al., 2022). A defining feature of SPL proteins is the presence of the SBP (SQUAMOSA Promoter-Binding Protein) domain a highly conserved DNA-binding domain comprising around 76 to 80 amino acids, featuring two zinc finger motifs and a nuclear localization signal (NLS) (Li et al., 2020a). The SBP domain specifically binds GTAC core motifs in the promoter regions of target genes, thereby modulating gene expression programs critical for plant growth (Birkenbihl et al., 2005).
The SPL gene family exhibits variation in size across different plant species. A. thaliana contains 16 SPL genes, while O. sativa has 19, and Zea mays possesses up to 31 SPL members (Wu and Poethig, 2006; Xie et al., 2006; Mao et al., 2016). These numbers reflect lineage-specific expansions and gene duplication events, which have contributed to both functional redundancy and divergence among SPL family members. Phylogenetic analyses have grouped SPLs into several distinct clades based on sequence similarity and domain architecture, suggesting evolutionary specialization (Sun et al., 2021; He et al., 2022). Although some SPL genes share overlapping functions, others have acquired unique roles in tissue- or stage-specific development (Zhang et al., 2025) (Table 1).
Table 1. Overview of SPL genes and their regulatory roles in plant architecture across species.
Post-transcriptional regulation plays a key role in SPL gene function, particularly through microRNAs such as miR156 and miR157 (Lee et al., 2022; Zhang et al., 2025). These conserved miRNAs target sites within the coding region or 3′ untranslated region (3′-UTR) of SPL transcripts, resulting in mRNA cleavage or translational repression (Zhu et al., 2022). In Arabidopsis, 10 out of 16 SPL genes are regulated by miR156, and similar patterns are observed in other species, including rice and maize (Wu and Poethig, 2006; Xie et al., 2006; Mao et al., 2016). The expression of miR156 is developmentally regulated high during early vegetative stages and declining as plants mature thus timing the activation of SPL genes that promote adult traits such as leaf complexity, shoot maturation, and floral induction (Song et al., 2020; Li et al., 2022). Functional studies have shown that specific SPLs, such as SPL9 and SPL15, act redundantly in controlling vegetative phase change. In contrast, others like SPL3, SPL4, and SPL5 specialize in promoting floral development, illustrating the functional divergence within this gene family (Wu and Poethig, 2006; Zhao et al., 2022b; Yan et al., 2024). In the past five years, research trends on SPLs in plants have been summarized in Figure 1. The figure highlights that miR156, plant architecture, abiotic stress, and hormones are key topics closely associated with SPL studies.
Figure 1. Visualization of research trends related to SPL genes in plants over the past five years using a term co-occurrence map of SPL studies using VOSviewer software version 1.620 (https://www.vosviewer.com/). The figure highlights miR156, plant architecture, abiotic stress, and hormonal regulation as major research themes closely associated with SPL studies. (accessed: 24 August 2025).
3 Regulation and functional integration of SPLs in leaf development
The expression of SPL genes is precisely regulated in both space and time to synchronize plant development. In general, SPL transcripts are low in juvenile tissues and accumulate progressively during vegetative growth, marking the transition to the adult phase. Spatially, different SPLs exhibit distinct expression patterns; some are preferentially expressed in shoot apices and young leaves, while others localize to reproductive meristems or vascular tissues. For instance, AtSPL10 is primarily expressed in leaf primordia and midveins in A. thaliana (Xu et al., 2025a), where it influences leaf polarity and curvature. In contrast, BrSPL9 exhibits broader expression in shoot and leaf tissues, affecting both phase change and morphogenesis in Brassica rapa (Wang et al., 2014).
The regulation of SPL expression is under tight developmental control, primarily through the age pathway mediated by miR156 (Jiao et al., 2010). During early vegetative growth, high levels of miR156 suppress SPL transcripts. As the plant ages, miR156 levels decline, allowing OsSPL expression to rise and promote adult traits such as leaf serration, curvature, and the initiation of reproductive development (Table 2). In addition to age, SPLs respond to hormonal and environmental cues (Song et al., 2023). In Arabidopsis, cytokinin has been shown to induce AtSPL10 expression through ARR1, integrating hormonal signals with developmental timing (Barrera-Rojas et al., 2020). Other hormones such as auxin and gibberellins (GA) also influence SPL activity, either by modulating miR156 levels or through interaction with SPL targets, suggesting a complex network of regulatory feedback in Pyrus (Song et al., 2020).
Table 2. Overview of SPL genes and their roles in biotic and abiotic stress responses.
SPLs function through both direct and indirect interactions with key transcriptional regulators involved in leaf patterning (Chen et al., 2010). For example, AtSPL10 modulates leaf curvature by interacting with the HD-ZIP III transcription factor REVOLUTA (REV), forming a module that coordinates adaxial-abaxial polarity (Xu et al., 2025a). AtSPL9 and AtSPL15 are known to regulate or interact with TCP TFs, which are critical in controlling leaf shape and cell senescence (Hyun et al., 2016). Furthermore, AtSPLs exhibit antagonistic or synergistic relationships with AtKNOX genes, which play roles in meristem maintenance and compound leaf development (Roth et al., 2018). Hormonal pathways converge on these interactions. Cytokinin promotes AtSPL expression via ARR1 (Barrera-Rojas et al., 2020), while auxin may counteract SPL-mediated processes during organ initiation (Liu et al., 2019). Together, these cross-regulatory interactions position SPLs as key integrators of developmental timing, environmental adaptation, and hormonal signaling in shaping leaf morphology (Figure 2).
Figure 2. A schematic model of SPL gene regulation and functional integration in leaf development. SPL expression is modulated by miR156, hormones (cytokinin, auxin, and GA), and transcription factors (REV, TCP, and KNOX), thereby coordinating developmental phase transitions, leaf polarity, and morphogenesis. The blue spheres indicating that they represent other regulatory genes that can either repress or enhance the expression of miR156/157.
4 SPLs in leaf curvature and morphogenesis
Leaf curvature is a fundamental architectural trait that determines the efficiency of light interception, gas exchange, and overall plant productivity (Tabusam et al., 2023). It results from differential cell growth along the adaxial (upper) and abaxial (lower) surfaces of the leaf, often governed by a complex regulatory network involving polarity genes, hormonal signaling, and transcriptional programs (Tang et al., 2009). In model species such as A. thaliana, recent studies have identified SPL TFs, particularly AtSPL10, as key regulators of leaf curvature, acting through both genetic and hormonal modules to control this finely tuned process (Xu et al., 2025a).
A pivotal study by Xu et al. (2025a) demonstrated that SPL10 interacts directly with REVOLUTA (REV), an HD-ZIP III transcription factor known to promote adaxial leaf identity. Through physical interaction and co-expression, AtSPL10 and REV form a regulatory module that coordinates adaxial–abaxial polarity and defines curvature outcomes. Overexpression of AtSPL10 in Arabidopsis resulted in severely curled leaves, whereas loss-of-function spl10 mutants partially rescued the curled-leaf phenotype in rev mutants, highlighting functional convergence. This genetic interaction mirrors earlier findings on HD-ZIP III (REV) and KANADI pathways, suggesting that SPLs operate within established polarity networks (Emery et al., 2003; Husbands et al., 2009). In addition, ZF-HD transcription factors, especially HB34, regulate shoot architecture in Arabidopsis by repressing miR157 and promoting the expression of its target gene, SPL10 (Lee et al., 2022).
Beyond its direct regulation of REVOLUTA (REV), BrSPL10 may influence broader leaf polarity pathways in Chinese cabbage (Xu et al., 2025a). Although SPL10 influences leaf morphology and polarity through regulatory modules involving REVOLUTA (REV), there is no evidence that SPL10 directly regulates abaxial determinant genes such as KANADI or YABBY. Any observed effects on leaf polarity are more likely mediated indirectly through REV- or BOP-dependent pathways (Gao et al., 2018; Hu et al., 2023).
The phenotypic consequences of SPL10 manipulation are striking: while overexpression results in upward-curled, narrow leaves, spl10 mutants display more flattened, expanded leaf blades. This phenotype is partially rescued in rev spl10 double mutants, confirming the antagonistic yet cooperative function of AtSPL10 and REV (Xu et al., 2025b). These findings parallel observations in other SPLs such as SPL9, which also contribute to morphogenetic traits, though with less direct influence on curvature. Comparative studies across species remain limited, but the regulatory logic appears conserved; for instance, BrpSPL9 in B. rapa affects heading time and leaf folding, possibly through similar polarity and growth control pathways (Wang et al., 2014). In addition, AGAMOUS-like MADS box protein 79 (AGL79) regulates plant development in a dose-dependent manner, affecting leaf morphology, shoot branching, and flowering. AtSPL10 directly activates it and acts downstream of the miR156/SPL10 module to influence lateral root growth (Gao et al., 2017).
Understanding the role of SPLs in leaf curvature has important implications for agriculture (Wang et al., 2022). In crops like rice and maize, optimal leaf angle, a trait closely tied to curvature and blade architecture, is critical for maximizing light interception and yield under dense planting. While most SPL research has been centered on Arabidopsis, translational insights are emerging (Li et al., 2020b). For example, OsSPL14 (IPA1), a gene regulated by OsmiR156, plays a crucial role in shaping the ideal plant architecture in rice by reducing tiller quantity, enhancing lodging resistance, and increasing grain yield (Jiao et al., 2010). Bridging these studies with knowledge from Arabidopsis SPL10-REV systems offers potential routes for engineering ideotype leaves with favorable curvature and angles for enhanced photosynthetic efficiency and crop improvement.
5 SPLs in leaf senescence and maturation
Leaf senescence is the final developmental stage of a leaf’s lifecycle, marked by coordinated processes such as chlorophyll degradation, nutrient remobilization, and programmed cell death (Guo et al., 2021; Ritonga et al., 2023). It is tightly regulated by both internal developmental cues and external environmental factors. Among the internal regulators, the miR156–SPL module has emerged as a central age-dependent mechanism that coordinates the timing of leaf maturation and senescence (Xu et al., 2016). In young plants, high levels of miR156 suppress the expression of its target SPL genes, maintaining juvenile traits and delaying aging. As the plant matures, miR156 levels decline, while miR172 levels increase, leading to the gradual activation of SPL transcription factors that promote adult-phase characteristics, including leaf ageing (Vander Schoor et al., 2022).
SPL9 is a key transcription factor involved in developmental phase change via the miR156–SPL module. To date, no studies have explicitly shown that SPL9 directly regulates ORE1, SAG29, or chlorophyll biosynthesis genes (Seo et al., 2011; Rauf et al., 2013). These senescence pathways may operate independently or downstream of other regulators. In contrast, SPL13 has been implicated in age-related developmental transitions, although its role in leaf senescence appears to be less pronounced than that of SPL9. Notably, recent findings suggest that AtSPL13 orthologs can respond to hormonal cues such as abscisic acid (ABA) and ethylene, potentially linking hormonal signals with age-related gene expression (Song et al., 2023).
Although direct evidence linking SPLs to nutrient remobilization is limited, SPL transcription factors, particularly SPL9 have been shown to regulate age-dependent developmental transitions and influence the expression of senescence-associated genes. These include genes involved in chlorophyll degradation and leaf maturation, highlighting their role in the timing and progression of leaf senescence. The upregulation of SPLs during later developmental stages reflects their function as phase identity markers, bridging the transition from juvenile to adult stages and reproductive competence. Collectively, current findings support SPLs, especially those regulated by the miR156 pathway, as essential components in the genetic network that integrates age cues with transcriptional regulation of senescence (Figure 3) (Xu et al., 2016).
Figure 3. Network of genes associated with SPL transcription factors and the miR156/miR172 regulatory modules in controlling leaf curvature and senescence. The figure illustrates how SPLs integrate age-related miRNA signaling with hormonal and transcriptional pathways to modulate leaf polarity, morphogenesis, and aging processes.
6 Crosstalk between SPLs and environmental signals
Plants constantly adjust their development in response to changing environmental conditions, and TFs, such as SPLs, serve as critical hubs that integrate internal genetic programs with external signals (Ritonga et al., 2021). Recent studies have shown that SPL gene expression and activity can be modulated by environmental factors, including light intensity, temperature fluctuations, and abiotic stressors such as drought, salinity, and nutrient limitation (Zhao et al., 2022b; Jing et al., 2025). Light-regulated developmental transitions, for instance, are partly mediated by changes in miR156 expression, which in turn affects the timing of SPL gene activation. Under extended photoperiods or high light conditions, a reduction in miR156 leads to increased SPL activity and the advancement of developmental events, such as leaf expansion and senescence (Cao et al., 2023).
Temperature extremes and abiotic stress also alter the function of SPL in leaves. Several SPLs, including SPL9 and SPL13, have been reported to participate in stress adaptation mechanisms, often through downstream targets involved in hormone signaling, redox regulation, and cell wall modification (LaFountain and Yuan, 2021; Ma et al., 2021; Zhao et al., 2022b). For example, under aluminum stress, SPL13 expression increases while miR156 is suppressed in alfalfa roots. Overexpression of miR156 leads to higher Al accumulation, membrane damage, and nutrient loss, whereas increased SPL13 enhances root length and Al tolerance. Transcriptome and ChIP-seq analyses revealed that SPL13 regulates genes involved in Al response, including transporters, transcription factors, and cell wall-associated proteins (Allam et al., 2025). Additionally, SPLs may indirectly mediate tolerance by modulating leaf structure and growth, enabling adjustments in leaf size, angle, or curvature to reduce water loss or optimize light capture under adverse conditions (Li et al., 2024; Bu et al., 2025). Furthermore, overexpression of BpmiR156 resulted in the transcriptional downregulation of BpSPL4 and BpSPL9, accompanied by differential expression of hormone-related genes involved in auxin and cytokinin biosynthesis, including BpARR3, BpARR11, and BpmiR172 (Yan et al., 2024).
At the molecular level, epigenetic and transcriptional reprogramming play a role in linking stress with SPL regulation. Environmental stress can affect histone modifications and DNA methylation at the MIR156 locus or SPL promoters, thereby shifting the expression thresholds of these genes reversibly (Bu et al., 2025). Moreover, SPLs themselves may be subject to transcriptional repression or activation by stress-induced transcription factors, such as DREB or WRKY family members, which are known to bind to the promoter regions of development-related genes (Zhao et al., 2022b). These layers of regulation enable a flexible and context-dependent role for SPLs in tuning leaf growth and developmental timing under environmental stress, underscoring their importance in shaping both plant form and resilience (Zheng et al., 2019; Jerome Jeyakumar et al., 2020).
7 SPLs in crop leaf development
While much of our mechanistic understanding of SPL TFs stems from studies in A. thaliana, recent research has expanded to include several economically important crops including rice, maize, wheat, barley and sorghum, revealing both conserved and specialized roles for SPLs in regulating leaf development, plant architecture, and yield-related traits (Liu et al., 2019; Giaume and Fornara, 2021; He et al., 2024; Zhong et al., 2024). In rice, SPL14 regulates leaf angle and tiller number, contributing to higher planting density and improved yield (Jiao et al., 2010). However, in another study, it was confirmed that OsSPL14 enhances rice grain appearance by reducing chalkiness through direct activation of Wx and PDIL1-1, key genes involved in starch and protein regulation. It also interacts with NF-Y transcription factors to promote their expression. Loss of OsSPL14 impairs endosperm development, highlighting its crucial role in improving grain quality (Li et al., 2025b). In maize (Zea mays), SPL genes such as ZmSPL12 have been linked to plant height, leaf width, and photosynthetic efficiency (Zhao et al., 2022a). In wheat (Triticum aestivum), SPL family members are involved in flag leaf morphology, influencing grain filling and biomass accumulation (Liu et al., 2019). Notably, in Chinese cabbage (Brassica rapa ssp. pekinensis), BrpSPL9 has been shown to regulate the earliness of heading time by affecting leaf incurvature, a key trait for head formation (Wang et al., 2014).
Given their central roles in leaf architecture, manipulation of SPL genes has emerged as a promising strategy for enhancing crop traits. CRISPR/Cas9-mediated modification of SPL genes has been successfully applied in crops such as tomato and soybean. In tomato, editing the SPL-CNR gene impaired fruit ripening, ethylene production, carotenoid accumulation, and volatile synthesis, confirming SPL-CNR’s central role in ripening regulation (Do et al., 2024). In soybean, simultaneous mutation of multiple GmSPL9 genes using CRISPR/Cas9 led to changes in node and branch number, demonstrating the potential of SPL gene editing to improve plant architecture and yield-related traits (Bao et al., 2019). In Chinese cabbage, altering BrpSPL9 expression can control heading time and leaf folding, which are crucial for market quality (Wang et al., 2014). Unfortunately, there is no published evidence of CRISPR/Cas9-mediated modification of SPL family genes in Chinese cabbage.
The biotechnological potential of SPLs extends beyond trait modification to the development of climate-resilient soybean. By targeting SPLs that interface with hormonal and environmental pathways, breeders can develop plants that adapt their leaf morphology to stress conditions such as drought or high planting density. Genome editing technologies, such as CRISPR/Cas9, offer precise tools to manipulate specific SPL loci without introducing foreign genes, thereby enhancing the acceptance of soybean in regulatory frameworks (Bao et al., 2019). As research continues to uncover the molecular targets and networks controlled by SPLs, these transcription factors emerge as valuable levers in designing next-generation rice, barley, wheat, sorghum with optimized canopy structure, enhanced photosynthetic efficiency, and improved yield potential.
8 Challenges and future perspectives
Despite significant advances in understanding the roles of SPL transcription factors, several challenges remain that limit the full exploitation of their potential in both basic research and crop improvement. Most current studies focus on a few well-characterized SPLs (e.g., SPL3, SPL9, SPL10, SPL14) in model plants like Arabidopsis and rice, leaving the functions of many other family members unexplored, especially in non-model and economically important species (Bu et al., 2025). Additionally, the phenotypic redundancy among SPL paralogs often masks loss-of-function effects, complicating the functional dissection (Preston and Hileman, 2010; 2013). Moreover, the molecular mechanisms linking SPL activity to cellular and tissue-level changes in leaf morphology are still incomplete, particularly regarding downstream targets, spatial specificity, and cross-regulatory feedback (Li et al., 2024).
To overcome these limitations, future research will benefit from integrated multi-omics and systems biology approaches, including transcriptomics, proteomics, epigenomics, and metabolomics (Tyagi et al., 2022). Such strategies can unravel the broader regulatory networks in which SPLs are embedded and identify dynamic changes during leaf development or in response to environmental conditions. Computational modeling, gene regulatory network mapping, and cell-type-specific expression profiling will also enhance our ability to predict SPL functions under diverse developmental and environmental conditions (Van den Broeck et al., 2020; Saint-André, 2021; Fu et al., 2024). These comprehensive approaches are especially important for translating findings from Arabidopsis to crops, where environmental variability and complex traits require a systems-level understanding.
The emergence of precise genome editing tools such as CRISPR/Cas9 has opened new avenues for SPL-based breeding strategies (Razzaq et al., 2021). By targeting individual SPL genes or their regulatory elements, such as miR156-binding sites or promoter regions, researchers can modulate leaf architecture traits in a controlled manner. Looking ahead, emerging research into non-coding RNAs, including long non-coding RNAs (lncRNAs) and circular RNAs (Liu et al., 2015; Zhang and Dai, 2022), suggests new layers of post-transcriptional SPL regulation that remain largely unexplored. Furthermore, post-translational modifications of SPL proteins, such as phosphorylation, ubiquitination, or interaction with chromatin remodelers, may fine-tune their stability and activity in a context-dependent manner (Li et al., 2025c). Expanding our knowledge in these areas will be critical for unlocking the full potential of SPLs as master regulators of leaf development and stress adaptation in crops.
9 Conclusion and future perspective
SQUAMOSA Promoter-Binding Protein-Like (SPL) transcription factors are central regulators of plant development, orchestrating genetic, hormonal, and environmental signals to shape plant architecture, flowering, and stress responses. Advances in functional genomics and molecular genetics have demonstrated the highly conserved yet functionally diverse roles of these fields across species, influencing critical traits such as vegetative-to-reproductive phase transitions, reproductive development, and tolerance to abiotic and biotic stresses. However, significant knowledge gaps remain, particularly in understanding species-specific SPL regulatory networks, their interactions with other transcription factors, and their evolutionary diversification in both crop and forestry species. Future research integrating high-resolution transcriptomics, advanced gene-editing technologies, and comparative genomics will be crucial to unlock the full potential of SPL genes in plant breeding. Harnessing SPL functions through targeted genetic engineering presents promising opportunities to optimize plant architecture, increase yield, and enhance resilience to climate change. By bridging molecular discoveries with applied breeding strategies and biotechnological innovation, SPL transcription factors can be transformed from fundamental research targets into practical tools for sustainable agriculture and forestry.
Author contributions
FR: Conceptualization, Visualization, Writing – original draft, Writing – review & editing. YX: Conceptualization, Visualization, Writing – original draft, Writing – review & editing. BC: Conceptualization, Visualization, Writing – original draft, Writing – review & editing. XL: Writing – review & editing. JG: Project administration, Writing – review & editing. JL: Conceptualization, Project administration, Writing – review & editing.
Funding
The author(s) declare financial support was received for the research and/or publication of this article. This research was funded by the Key R&D Program of Shandong Province, China (2023LZGC014, 2024KJHZ005, 2024LZGC03602), the Shandong Agriculture Research System, China (SDARS-05), the Project of 20 New Items for Universities in Jinan, Shandong (202228058), the China Agriculture Research System (CARS-23-G13), the 2022 Tai 'an Agricultural Superior Seed Project (2022NYLZ07), the Agricultural Science and Technology Innovation Project of Shandong Academy of Agricultural Sciences (CXGC2025C08), and the National Natural Science Foundation, China (32172591).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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References
Allam, G., Sakariyahu, S. K., Shan, B., Aung, B., McDowell, T., Papadopoulos, Y., et al. (2025). Aluminum Stress Response Is Regulated Through a miR156/SPL13 Module in Medicago sativa. Genes. 16, 751. doi: 10.3390/genes16070751
Bao, A., Chen, H., Chen, L., Chen, S., Hao, Q., Guo, W., et al. (2019). CRISPR/Cas9-mediated targeted mutagenesis of GmSPL9 genes alters plant architecture in soybean. BMC Plant Biol. 19, 131. doi: 10.1186/s12870-019-1746-6
Barrera-Rojas, C. H., Rocha, G. H. B., Polverari, L., Pinheiro Brito, D. A., Batista, D. S., Notini, M. M., et al. (2020). miR156-targeted SPL10 controls Arabidopsis root meristem activity and root-derived de novo shoot regeneration via cytokinin responses. J. Exp. Bot. 71, 934–950. doi: 10.1093/jxb/erz475
Birkenbihl, R. P., Jach, G., Saedler, H., and Huijser, P. (2005). Functional dissection of the plant-specific SBP-domain: overlap of the DNA-binding and nuclear localization domains. J. Mol. Biol. 352, 585–596. doi: 10.1016/j.jmb.2005.07.013
Bu, R., Qiu, Z., Dong, J., Chen, L., Zhou, Y., Wang, H., et al. (2025). The role of SQUAMOSA-PROMOTER BINDING PROTEIN-like (SPL) transcription factors in plant growth and environmental stress response: A comprehensive review of recent advances. Horticulturae. 11, 584. doi: 10.3390/horticulturae11060584
Cao, R., Guo, L., Ma, M., Zhang, W., Liu, X., and Zhao, H. (2019). Identification and functional characterization of squamosa promoter binding protein-like gene taSPL16 in wheat (Triticum aestivum L.). Front. Plant Sci. 10. doi: 10.3389/fpls.2019.00212
Cao, J., Liu, H., Tan, S., and Li, Z. (2023). Transcription factors-regulated leaf senescence: current knowledge, challenges and approaches. Int. J. Mol. Sci. 24, 9245. doi: 10.3390/ijms24119245
Chao, L.-M., Liu, Y.-Q., Chen, D.-Y., Xue, X.-Y., Mao, Y.-B., and Chen, X.-Y. (2017). Arabidopsis transcription factors SPL1 and SPL12 confer plant thermotolerance at reproductive stage. Mol. Plant 10, 735–748. doi: 10.1016/j.molp.2017.03.010
Chen, X., Zhang, Z., Liu, D., Zhang, K., Li, A., and Mao, L. (2010). SQUAMOSA promoter-binding protein-like transcription factors: star players for plant growth and development. J. Integr. Plant Biol. 52, 946–951. doi: 10.1111/j.1744-7909.2010.00987.x
Chopy, M., Binaghi, M., Cannarozzi, G., Halitschke, R., Boachon, B., Heutink, R., et al. (2023). A single MYB transcription factor with multiple functions during flower development. New Phytol. 239, 2007–2025. doi: 10.1111/nph.19096
Do, H., Chung, M.-Y., Cho, W., Kim, S.-T., Lee, S.-B., and Lee, J. M. (2024). CRISPR/Cas9-edited SPL-CNR quantitatively control tomato fruit ripening. Sci. Hortic. 330, 113073. doi: 10.1016/j.scienta.2024.113073
Dong, H., Yan, S., Jing, Y., Yang, R., Zhang, Y., Zhou, Y., et al. (2021). MIR156-targeted SPL9 is phosphorylated by SnRK2s and interacts with ABI5 to enhance ABA responses in Arabidopsis. Front. Plant Sci. 12, 708573. doi: 10.3389/fpls.2021.708573
Emery, J. F., Floyd, S. K., Alvarez, J., Eshed, Y., Hawker, N. P., Izhaki, A., et al. (2003). Radial patterning of arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13, 1768–1774. doi: 10.1016/j.cub.2003.09.035
Fu, J., McKinley, B., James, B., Chrisler, W., Markillie, L. M., Gaffrey, M. J., et al. (2024). Cell-type-specific transcriptomics uncovers spatial regulatory networks in bioenergy sorghum stems. Plant J. 118, 1668–1688. doi: 10.1111/tpj.16690
Gao, R., Wang, Y., Gruber, M. Y., and Hannoufa, A. (2017). miR156/SPL10 modulates lateral root development, branching and leaf morphology in arabidopsis by silencing AGAMOUS-LIKE 79. Front. Plant Sci. 8, 2226. doi: 10.3389/fpls.2017.02226
Gao, R., Wang, Y., Gruber, M. Y., and Hannoufa, A. (2018). miR156/SPL10 modulates lateral root development, branching and leaf morphology in arabidopsis by silencing AGAMOUS-LIKE 79. Front. Plant Sci. 8. doi: 10.3389/fpls.2017.02226
Giaume, F. and Fornara, F. (2021). SPL transcription factors prevent inflorescence reversion in rice. Mol. Plant 14, 1041–1043. doi: 10.1016/j.molp.2021.06.009
Guo, Y., Ren, G., Zhang, K., Li, Z., Miao, Y., and Guo, H. (2021). Leaf senescence: progression, regulation, and application. Mol. Horticulture. 1, 5. doi: 10.1186/s43897-021-00006-9
He, F., Long, R., Wei, C., Zhang, Y., Li, M., Kang, J., et al. (2022). Genome-wide identification, phylogeny and expression analysis of the SPL gene family and its important role in salt stress in Medicago sativa L. BMC Plant Biol. 22, 295. doi: 10.1186/s12870-022-03678-7
He, A., Zhou, H., Ma, C., Bai, Q., Yang, H., Yao, X., et al. (2024). Genome-wide identification and expression analysis of the SPL gene family and its response to abiotic stress in barley (Hordeum vulgare L.). BMC Genomics 25, 846. doi: 10.1186/s12864-024-10773-6
Hu, T., Manuela, D., and Xu, M. (2023). SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 9 and 13 repress BLADE-ON-PETIOLE 1 and 2 directly to promote adult leaf morphology in Arabidopsis. J. Exp. Bot. 74, 1926–1939. doi: 10.1093/jxb/erad017
Huang, J., Zhao, X., Bürger, M., Wang, Y., and Chory, J. (2021). Two interacting ethylene response factors regulate heat stress response. Plant Cell. 33, 338–357. doi: 10.1093/plcell/koaa026
Husbands, A. Y., Chitwood, D. H., Plavskin, Y., and Timmermans, M. C. (2009). Signals and prepatterns: new insights into organ polarity in plants. Genes Dev. 23, 1986–1997. doi: 10.1101/gad.1819909
Hyun, Y., Richter, R., Vincent, C., Martinez-Gallegos, R., Porri, A., and Coupland, G. (2016). Multi-layered regulation of SPL15 and cooperation with SOC1 integrate endogenous flowering pathways at the arabidopsis shoot meristem. Dev. Cell. 37, 254–266. doi: 10.1016/j.devcel.2016.04.001
Jadhao, K. R., Kale, S. S., Chavan, N. S., and Janjal, P. H. (2023). Genome-wide analysis of the SPL transcription factor family and its response to water stress in sunflower (Helianthus annuus). Cell Stress Chaperones. 28, 943–958. doi: 10.1007/s12192-023-01388-z
Jerome Jeyakumar, J. M., Ali, A., Wang, W. M., and Thiruvengadam, M. (2020). Characterizing the role of the miR156-SPL network in plant development and stress response. Plants (Basel). 9, 1206. doi: 10.3390/plants9091206
Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., Liu, G., et al. (2010). Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541–544. doi: 10.1038/ng.591
Jing, X., Wang, D., Liu, X., Chen, G., Guo, X., Wang, X.-F., et al. (2025). The SBP transcription factor MdSPL13B positively regulates salt tolerance in apple. Hortic. Plant J. doi: 10.1016/j.hpj.2025.01.008
John, S., Apelt, F., Kumar, A., Acosta, I. F., Bents, D., Annunziata, M. G., et al. (2024). The transcription factor HSFA7b controls thermomemory at the shoot apical meristem by regulating ethylene biosynthesis and signaling in Arabidopsis. Plant Commun. 5, 100743. doi: 10.1016/j.xplc.2023.100743
Khoso, M. A., Hussain, A., Ritonga, F. N., Ali, Q., Channa, M. M., Alshegaihi, R. M., et al. (2022). WRKY transcription factors (TFs): Molecular switches to regulate drought, temperature, and salinity stresses in plants. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.1039329
Kong, D., Xu, M., Liu, S., Liu, T., Liu, B., Wang, X., et al. (2025). Genome-wide identification and expression profiling of the SPL transcription factor family in response to abiotic stress in centipedegrass. Plants. 14, 62. doi: 10.3390/plants14010062
LaFountain, A. M. and Yuan, Y.-W. (2021). Repressors of anthocyanin biosynthesis. New Phytol. 231, 933–949. doi: 10.1111/nph.17397
Lee, Y. K., Kumari, S., Olson, A., Hauser, F., and Ware, D. (2022). Role of a ZF-HD transcription factor in miR157-mediated feed-forward regulatory module that determines plant architecture in arabidopsis. Int. J. Mol. Sci. 23, 8665. doi: 10.3390/ijms23158665
Li, Y., Deng, Y., Qin, D., and An, X. (2025a). Study of the SPL gene family and miR156-SPL module in Populus tomentosa: Potential roles in juvenile-to-adult phase transition and reproductive phase. Int. J. Biol. Macromol. 296, 139547. doi: 10.1016/j.ijbiomac.2025.139547
Li, Y., Guo, X., Song, J., Xu, K., Qin, T., Zhang, X., et al. (2025b). OsSPL14 and OsNF-YB9/YC8–12 subunits cooperate to enhance grain appearance quality by promoting Waxy and PDIL1–1 expression in rice. Plant Commun. 6, 101348. doi: 10.1016/j.xplc.2025.101348
Li, M., He, Q., Zhang, Y., Sun, B., Luo, Y., Zhang, Y., et al. (2020a). New insights into the evolution of the SBP-box family and expression analysis of genes in the growth and development of Brassica juncea. Biotechnol. Biotechnol. Equip. 34, 810–824. doi: 10.1080/13102818.2020.1803131
Li, X.-M., Jenke, H., Strauss, S., Bazakos, C., Mosca, G., Lymbouridou, R., et al. (2024). Cell-cycle-linked growth reprogramming encodes developmental time into leaf morphogenesis. Curr. Biol. 34, 541–556.e515. doi: 10.1016/j.cub.2023.12.050
Li, Z., Qin, L., Wang, D., Cui, T., Liang, Y., Zang, S., et al. (2025c). Protein post-translational modification in plants: Regulation and beyond. Hortic. Plant J. doi: 10.1016/j.hpj.2025.02.003
Li, L., Shi, F., Wang, G., Guan, Y., Zhang, Y., Chen, M., et al. (2022). Conservation and divergence of SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family between wheat and rice. Int. J. Mol. Sci. 23, 2099. doi: 10.3390/ijms23042099
Li, X., Wu, P., Lu, Y., Guo, S., Zhong, Z., Shen, R., et al. (2020b). Synergistic interaction of phytohormones in determining leaf angle in crops. Int. J. Mol. Sci. 21, 5052. doi: 10.3390/ijms21145052
Liu, K., Cao, J., Yu, K., Liu, X., Gao, Y., Chen, Q., et al. (2019). Wheat taSPL8 modulates leaf angle through auxin and brassinosteroid signaling. Plant Physiol. 181, 179–194. doi: 10.1104/pp.19.00248
Liu, X., Hao, L., Li, D., Zhu, L., and Hu, S. (2015). Long non-coding RNAs and their biological roles in plants. Genomics Proteomics Bioinf. 13, 137–147. doi: 10.1016/j.gpb.2015.02.003
Ma, Y., Xue, H., Zhang, F., Jiang, Q., Yang, S., Yue, P., et al. (2021). The miR156/SPL module regulates apple salt stress tolerance by activating MdWRKY100 expression. Plant Biotechnol. J. 19, 311–323. doi: 10.1111/pbi.13464
Mao, H.-D., Yu, L.-J., Li, Z.-J., Yan, Y., Han, R., Liu, H., et al. (2016). Genome-wide analysis of the SPL family transcription factors and their responses to abiotic stresses in maize. Plant Gene. 6, 1–12. doi: 10.1016/j.plgene.2016.03.003
Nikolopoulos, D., Bresta, P., Daliani, V., Haghiou, V., Darra, N., Liati, M., et al. (2024). Leaf anatomy affects optical properties and enhances photosynthetic performance under oblique light. Plant Cell Environment. 47, 1471–1485. doi: 10.1111/pce.14823
Preston, J. C. and Hileman, L. C. (2010). SQUAMOSA-PROMOTER BINDING PROTEIN 1 initiates flowering in Antirrhinum majus through the activation of meristem identity genes. Plant J. 62, 704–712. doi: 10.1111/j.1365-313X.2010.04184.x
Preston, J. C. and Hileman, L. C. (2013). Functional evolution in the plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family. Front. Plant Sci. 4. doi: 10.3389/fpls.2013.00080
Rahimi, A., Karami, O., Balazadeh, S., and Offringa, R. (2022). miR156-independent repression of the ageing pathway by longevity-promoting AHL proteins in Arabidopsis. New Phytol. 235, 2424–2438. doi: 10.1111/nph.18292
Rauf, M., Arif, M., Dortay, H., Matallana-Ramírez, L. P., Waters, M. T., Gil Nam, H., et al. (2013). ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription. EMBO Rep. 14, 382–388. doi: 10.1038/embor.2013.24
Razzaq, M. K., Aleem, M., Mansoor, S., Khan, M. A., Rauf, S., Iqbal, S., et al. (2021). Omics and CRISPR-cas9 approaches for molecular insight, functional gene analysis, and stress tolerance development in crops. Int. J. Mol. Sci. 22, 1292. doi: 10.3390/ijms22031292
Ren, Y., Ma, R., Fan, Y., Zhao, B., Cheng, P., Fan, Y., et al. (2022). Genome-wide identification and expression analysis of the SPL transcription factor family and its response to abiotic stress in Quinoa (Chenopodium quinoa). BMC Genomics 23, 773. doi: 10.1186/s12864-022-08977-9
Ritonga, F. N., Ngatia, J. N., Wang, Y., Khoso, M. A., Farooq, U., and Chen, S. (2021). AP2/ERF, an important cold stress-related transcription factor family in plants: A review. Physiol. Mol. Biol. Plants. 27, 1953–1968. doi: 10.1007/s12298-021-01061-8
Ritonga, F. N., Zhou, D., Zhang, Y., Song, R., Li, C., Li, J., et al. (2023). The roles of gibberellins in regulating leaf development. Plants (Basel). 12, 1953–1968. doi: 10.3390/plants12061243
Roth, O., Alvarez, J. P., Levy, M., Bowman, J. L., Ori, N., and Shani, E. (2018). The KNOXI transcription factor SHOOT MERISTEMLESS regulates floral fate in arabidopsis. Plant Cell. 30, 1309–1321. doi: 10.1105/tpc.18.00222
Saint-André, V. (2021). Computational biology approaches for mapping transcriptional regulatory networks. Comput. Struct. Biotechnol. J. 19, 4884–4895. doi: 10.1016/j.csbj.2021.08.028
Seo, P. J., Park, J. M., Kang, S. K., Kim, S. G., and Park, C. M. (2011). An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta 233, 189–200. doi: 10.1007/s00425-010-1293-8
Song, M., Li, A., Sun, L., Mei, Y., Wang, Z., Wang, R., et al. (2023). The miR156x + p/SPL13–6 module responds to ABA, IAA, and ethylene, and SPL13–6 participates in the juvenile–adult phase transition in Pyrus. Horticulture Environment Biotechnol. 64, 437–448. doi: 10.1007/s13580-022-00482-y
Song, M., Wang, R., Zhou, F., Wang, R., Zhang, S., Li, D., et al. (2020). SPLs-mediated flowering regulation and hormone biosynthesis and signaling accompany juvenile-adult phase transition in Pyrus. Sci. Hortic. 272, 109584. doi: 10.1016/j.scienta.2020.109584
Sun, H., Mei, J., Zhao, W., Hou, W., Zhang, Y., Xu, T., et al. (2021). Phylogenetic analysis of the SQUAMOSA promoter-binding protein-like genes in four ipomoea species and expression profiling of the ibSPLs during storage root development in sweet potato (Ipomoea batatas). Front. Plant Sci. 12. doi: 10.3389/fpls.2021.801061
Sun, X., Zhang, L., Xu, W., Zheng, J., Yan, M., Zhao, M., et al. (2024). A comprehensive analysis of the peanut SQUAMOSA promoter binding protein-like gene family and how ahSPL5 enhances salt tolerance in transgenic arabidopsis. Plants 13, 801061. doi: 10.3390/plants13081057
Tabusam, J., Liu, M., Luo, L., Zulfiqar, S., Shen, S., Ma, W., et al. (2023). Physiological control and genetic basis of leaf curvature and heading in brassica rapa L. J. Advanced Res. 53, 49–59. doi: 10.1016/j.jare.2022.12.010
Tang, L., Shi, C.-L., Zhu, Y., Jing, Q., and Cao, W.-X. (2009). A quantitative analysis on leaf curvature characteristics in rice. Crop Modeling and Decision Support. 71–76. doi: 10.1007/978-3-642-01132-0_8
Tyagi, P., Singh, D., Mathur, S., Singh, A., and Ranjan, R. (2022). Upcoming progress of transcriptomics studies on plants: An overview. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.1030890
Van den Broeck, L., Gordon, M., Inzé, D., Williams, C., and Sozzani, R. (2020). Gene regulatory network inference: connecting plant biology and mathematical modeling. Front. Genet. 11. doi: 10.3389/fgene.2020.00457
Vander Schoor, J. K., Hecht, V., Aubert, G., Burstin, J., and Weller, J. L. (2022). Defining the components of the miRNA156-SPL-miR172 aging pathway in pea and their expression relative to changes in leaf morphology. Plant Gene. 30, 100354. doi: 10.1016/j.plgene.2022.100354
Wang, Y., Hu, Z., Yang, Y., Chen, X., and Chen, G. (2009). Function annotation of an SBP-box gene in Arabidopsis based on analysis of co-expression networks and promoters. Int. J. Mol. Sci. 10, 116–132. doi: 10.3390/ijms10010116
Wang, M., Lavelle, D., Yu, C., Zhang, W., Chen, J., Wang, X., et al. (2022). The upregulated LsKN1 gene transforms pinnately to palmately lobed leaves through auxin, gibberellin, and leaf dorsiventrality pathways in lettuce. Plant Biotechnol. J. 20, 1756–1769. doi: 10.1111/pbi.13861
Wang, L., Ming, L., Liao, K., Xia, C., Sun, S., Chang, Y., et al. (2021). Bract suppression regulated by the miR156/529-SPLs-NL1-PLA1 module is required for the transition from vegetative to reproductive branching in rice. Mol. Plant 14, 1168–1184. doi: 10.1016/j.molp.2021.04.013
Wang, H. and Wang, H. (2015). The miR156/SPL Module, a Regulatory Hub and Versatile Toolbox, Gears up Crops for Enhanced Agronomic Traits. Mol. Plant 8, 677–688. doi: 10.1016/j.molp.2015.01.008
Wang, Y., Wu, F., Bai, J., and He, Y. (2014). BrpSPL9 (Brassica rapa ssp. pekinensis SPL9) controls the earliness of heading time in Chinese cabbage. Plant Biotechnol. J. 12, 312–321. doi: 10.1111/pbi.12138
Wu, G. and Poethig, R. S. (2006). Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133, 3539–3547. doi: 10.1242/dev.02521
Wu, J.-w., Zhao, Z.-y., Hu, R.-c., and Huang, Y.-f. (2024). Genome-wide identification, stress-and hormone-responsive expression characteristics, and regulatory pattern analysis of Scutellaria baicalensis SbSPLs. Plant Mol. Biol. 114, 20. doi: 10.1007/s11103-023-01410-z
Xie, K., Wu, C., and Xiong, L. (2006). Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol. 142, 280–293. doi: 10.1104/pp.106.084475
Xu, M., Hu, T., Zhao, J., Park, M. Y., Earley, K. W., Wu, G., et al. (2016). Developmental Functions of miR156-Regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana. PloS Genet. 12, e1006263. doi: 10.1371/journal.pgen.1006263
Xu, P., Wan, Q., Shao, W., Wu, Y., Wu, F., Li, X., et al. (2025a). Orchestration of leaf curvature by the SBP transcription factor SPL10-REVOLUTA module in Arabidopsis. J. Integr. Plant Biol. 67, 1805–1822. doi: 10.1111/jipb.13893
Xu, P., Wan, Q., Shao, W., Wu, Y., Wu, F., Li, X., et al. (2025b). Orchestration of leaf curvature by the SBP transcription factor SPL10–REVOLUTA module in Arabidopsis. J. Integr. Plant Biol. 67, 1805–1822. doi: 10.1111/jipb.13893
Xue, G., Wu, W., Fan, Y., Ma, C., Xiong, R., Bai, Q., et al. (2024). Genome-wide identification, evolution, and role of SPL gene family in beet (Beta vulgaris L.) under cold stress. BMC Genomics 25, 101. doi: 10.1186/s12864-024-09995-5
Yan, B., Li, F., Ma, Q., Shen, T., Jiang, J., and Li, H. (2024). The miR156-SPL4/SPL9 module regulates leaf and lateral branch development in Betula platyphylla. Plant Sci. 338, 111869. doi: 10.1016/j.plantsci.2023.111869
Zhang, P. and Dai, M. (2022). CircRNA: a rising star in plant biology. J. Genet. Genomics 49, 1081–1092. doi: 10.1016/j.jgg.2022.05.004
Zhang, Y., Hu, Q., Zhai, X., Tu, Z., Wang, J., Wang, M., et al. (2024). Genome-wide investigation of SQUAMOSA promoter binding protein-like genes in Liriodendron and functional characterization of LcSPL2. AOB Plants 16, plae008. doi: 10.1093/aobpla/plae008
Zhang, L.-L., Huang, Y.-Y., Zheng, Y.-P., Liu, X.-X., Zhou, S.-X., Yang, X.-M., et al. (2022). Osa-miR535 targets SQUAMOSA promoter binding protein-like 4 to regulate blast disease resistance in rice. Plant J. 110, 166–178. doi: 10.1111/tpj.15663
Zhang, Y., Ni, X., Fu, X., Taheri, A., Zhang, W., Liu, P., et al. (2025). Comprehensive analysis of SPL gene family and miR156a/SPLs in the regulation of terpenoid indole alkaloid biosynthesis in Catharanthus roseus L. BMC Plant Biol. 25, 817. doi: 10.1186/s12870-025-06802-5
Zhang, H., Zhai, J., Mo, J., Li, D., and Song, F. (2012). Overexpression of rice sphingosine-1-phoshpate lyase gene OsSPL1 in transgenic tobacco reduces salt and oxidative stress tolerance. J. Integr. Plant Biol. 54, 652–662. doi: 10.1111/j.1744-7909.2012.01150.x
Zhao, Y., He, J., Liu, M., Miao, J., Ma, C., Feng, Y., et al. (2024). The SPL transcription factor TaSPL6 negatively regulates drought stress response in wheat. Plant Physiol. Biochem. 206, 108264. doi: 10.1016/j.plaphy.2023.108264
Zhao, J., Shi, M., Yu, J., and Guo, C. (2022b). SPL9 mediates freezing tolerance by directly regulating the expression of CBF2 in Arabidopsis thaliana. BMC Plant Biol. 22, 59. doi: 10.1186/s12870-022-03445-8
Zhao, B., Xu, M., Zhao, Y., Li, Y., Xu, H., Li, C., et al. (2022a). Overexpression of ZmSPL12 confers enhanced lodging resistance through transcriptional regulation of D1 in maize. Plant Biotechnol. J. 20, 622–624. doi: 10.1111/pbi.13787
Zheng, C., Ye, M., Sang, M., and Wu, R. (2019). A Regulatory Network for miR156-SPL Module in Arabidopsis thaliana. Int. J. Mol. Sci. 20, 6166. doi: 10.3390/ijms20246166
Zheng, L., Zhang, W., Wei, L., Li, M., and Liu, L. (2025). Functional characterization of maSPL8 reveals its different roles in biotic and abiotic stress responses in mulberry. Plants. 14, 950. doi: 10.3390/plants14060950
Zhong, Z., Zhong, L., Zhu, X., Jiang, Y., Zheng, Y., Lan, T., et al. (2024). Transcription factor OsSPL10 interacts with OsJAmyb to regulate blast resistance in rice. Crop J. 12, 301–307. doi: 10.1016/j.cj.2023.10.015
Keywords: leaf development, miR156, plant architecture, SPL transcription factors, stress response
Citation: Ritonga FN, Xu Y, Cui B, Liu X, Gao J and Li J (2025) Unraveling the multifaceted roles of SPL transcription factors in leaf development. Front. Plant Sci. 16:1696036. doi: 10.3389/fpls.2025.1696036
Received: 31 August 2025; Accepted: 28 October 2025;
Published: 19 November 2025.
Edited by:
Angela Roberta Lo Piero, University of Catania, ItalyReviewed by:
Jorge Londoño, University of Quindío, ColombiaPushpalatha Ganesh, Centurion University of Technology and Management, India
Copyright © 2025 Ritonga, Xu, Cui, Liu, Gao 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.
*Correspondence: Jingjuan Li, bGlqajA2MjBAMTYzLmNvbQ==
†These authors have contributed equally to this work