Roles of miR319 and TCP Transcription Factors in Leaf Development

Abstract

Sophisticated regulation of gene expression, including microRNAs (miRNAs) and their target genes, is required for leaf differentiation, growth, and senescence. The impact of miR319 and its target TEOSINTE BRANCHED1, CYCLOIDEA, and PROLIFERATING CELL NUCLEAR ANTIGEN BINDING FACTOR (TCP) genes on leaf development has been extensively investigated, but the redundancies of these gene families often interfere with the evaluation of their function and regulation in the developmental context. Here, we present the genetic evidence of the involvement of the MIR319 and TCP gene families in Arabidopsis (Arabidopsis thaliana) leaf development. Single mutations in MIR319A and MIR319B genes moderately inhibited the formation of leaf serrations, whereas double mutations increased the extent of this inhibition and resulted in the formation of smooth leaves. Mutations in MIR319 and gain-of-function mutations in the TCP4 gene conferred resistance against miR319 and impaired the cotyledon boundary and leaf serration formation. These mutations functionally associated with CUP-SHAPED COTYLEDON genes, which regulate the cotyledon boundary and leaf serration formation. In contrast, loss-of-function mutations in miR319-targeted and nontargeted TCP genes cooperatively induced the formation of serrated leaves in addition to changes in the levels of their downstream gene transcript. Taken together, these findings demonstrate that the MIR319 and TCP gene families underlie robust and multilayer control of leaf development. This study also provides a framework toward future researches on redundant miRNAs and transcription factors in Arabidopsis and crop plants.

Heteroexpression of Osa-miR319b improved switchgrass biomass yield and feedstock quality by repression of PvPCF5

“…Enhancing tiller density, height and/or reducing stem lignin content by biotechnology methods could effectively improve switchgrass biofuel characteristics [21,37]. MiR319-TCP module has been demonstrated to play a key role in plant development, such as promoting cell proliferation during leaf organ morphogenesis [22][23][24][25][26], delaying leaf senescence [27] and affecting flower development [28]. However, little is known about the biological function of miR319-TCP module in regulating stem development of perennial biofuel grasses, such as switchgrass.…”

“…In recent decades, several miRNAs and/or their target genes have been shown as potential molecular tools in improving biomass and/or saccharification efficiency in switchgrass by indirectly regulating plant development [20,21]. MiR319, one of the most ancient miRNAs, was reported to post-transcriptionally regulate mRNA abundance of class II TCP (TEOSINTE BRANCHED1, CYCLODEA, PROLIFERATING FACTORS/PCF) transcription factors [22][23][24][25][26]. Higher miR319 level or lower TCPs content resulted in an excess of cell proliferation generation crinkled or wider leaves by regulating plant cell proliferation and elongation [22][23][24][25][26], delayed leaf senescence by repressing jasmonic acid (JA) biosynthesis [27], and affected flower development [28].…”

“…MiR319, one of the most ancient miRNAs, was reported to post-transcriptionally regulate mRNA abundance of class II TCP (TEOSINTE BRANCHED1, CYCLODEA, PROLIFERATING FACTORS/PCF) transcription factors [22][23][24][25][26]. Higher miR319 level or lower TCPs content resulted in an excess of cell proliferation generation crinkled or wider leaves by regulating plant cell proliferation and elongation [22][23][24][25][26], delayed leaf senescence by repressing jasmonic acid (JA) biosynthesis [27], and affected flower development [28]. In Arabidopsis, the miR319-target class II TCPs, notably AtTCP4, have been reported to perform its biological function by activating cyclin-dependent kinase inhibitor 1 (ICK1) [29], DWARF4 (brassinolide (BR) biosynthesis key enzyme) [30] and LOX2 (lipoxygenase 2, a JA biosynthesis rate-limiting enzyme) [27].…”

“…To date, miR319-TCP module alterations to plant morphology focus mainly on leaf or flower [22][23][24][25][26][27][28], there are rare reports studying stem development characteristics, especially biofuel characteristics of stems. In this study, transgenic plants of overexpression of miR319 (OE-miR319), repression of miR319 (MIM319) and suppression of PvPCF5 activity were used to investigate the roles that miR319-PvPCF5 plays in regulating stem biomass yield and feedstock quality in switchgrass.…”

TCP7 functions redundantly with several Class I TCPs and regulates endoreplication in Arabidopsis

“…The plant-specific Arabidopsis TCP (TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FAC-TOR) transcription factor family is divided into two subfamilies, class I (13 members) and class II (11 members). These proteins function in the regulation of cell division and cell differentiation, flowering, hormone signaling, circadian rhythms, and organ formation (Martin-Trillo and Cubas 2010;Manassero et al 2013;Danisman 2016;Nicolas and Cubas 2016;Koyama et al 2017;Kubota et al 2017;Lucero et al 2017;Bresso et al 2018;Sarvepalli and Nath 2018;Vadde et al 2018;Zhou et al 2018).…”