miR319-Regulated TCP3 Modulates Silique Development Associated with Seed Shattering in Brassicaceae

Abstract

Seed shattering is an undesirable trait that leads to crop yield loss. Improving silique resistance to shattering is critical for grain and oil crops. In this study, we found that miR319-targeted TEOSINTE BRANCHED 1, CYCLOIDEA, and PROLIFERATING CELL NUCLEAR ANTIGEN BINDING FACTOR (TCPs) inhibited the process of post-fertilized fruits (silique) elongation and dehiscence via regulation of FRUITFULL (FUL) expression in Arabidopsis thaliana and Brassica napus. AtMIR319a activation resulted in a longer silique with thickened and lignified replum, whereas overexpression of an miR319a-resistant version of AtTCP3 (mTCP3) led to a short silique with narrow and less lignified replum. Further genetic and expressional analysis suggested that FUL acted downstream of TCP3 to negatively regulate silique development. Moreover, hyper-activation of BnTCP3.A8, a B. napus homolog of AtTCP3, in rapeseed resulted in an enhanced silique resistance to shattering due to attenuated replum development. Taken together, our findings advance our knowledge of TCP-regulated silique development and provide a potential target for genetic manipulation to reduce silique shattering in Brassica crops.

TCP Transcription Factors in Plant Reproductive Development: Juggling Multiple Roles

“…This study also suggested the participation of additional TCPs from both classes in the process, which deserves further investigation. In this sense, it was recently reported that in Arabidopsis jaw-D plants, in which the expression of several CIN TCPs is reduced as a consequence of miR319 overexpression, the silique replum is enlarged relative to that of wild-type plants, and the same happens when a dominant repressor form of the CIN protein AtTCP3 (AtTCP3-SRDX) is expressed from its own gene promoter [104]. Contrary to that, increased expression of AtTCP3 or its putative Brassica napus ortholog in the respective species reduces replum width and lignification, conferring increased resistance to shattering [104].…”

“…In this sense, it was recently reported that in Arabidopsis jaw-D plants, in which the expression of several CIN TCPs is reduced as a consequence of miR319 overexpression, the silique replum is enlarged relative to that of wild-type plants, and the same happens when a dominant repressor form of the CIN protein AtTCP3 (AtTCP3-SRDX) is expressed from its own gene promoter [104]. Contrary to that, increased expression of AtTCP3 or its putative Brassica napus ortholog in the respective species reduces replum width and lignification, conferring increased resistance to shattering [104]. In addition, CIN TCPs were related to ovule development since overexpression of either AtTCP3 or AtTCP5 causes ovule abortion, and loss of function of multiple CIN TCP genes disrupts ovule initiation and arrangement [105].…”

Novel quantitative trait loci from an interspecific Brassica rapa derivative improve pod shatter resistance in Brassica napus

“…The functionality of some of Arabidopsis pod dehiscence genes has also been demonstrated in Brassica species via overexpression, RNAi, gene editing, and induced mutation studies ( Ostergaard et al., 2006 ; Kord et al., 2015 ; Lawrenson et al., 2015 ; Braatz et al., 2018a ; Braatz et al., 2018b ; Stephenson et al., 2019 ; Li et al., 2021 ). Recently, it has also been shown that miR319-targeted TEOSINTE BRANCHED 1 , CYCLOIDEA , and PROFEERATIN CELL NUCLEAR ANTIGEN BINDING FACTOR ( TCPs ) inhibit pod elongation and dehiscence via regulation of FUL expression in A. thaliana and B. napus ( Cao et al., 2022 ). Although the network of pod dehiscence genes has been investigated in Arabidopsis, their expression level has not been fine-tuned in commercial canola varieties with genetic modification approaches, except in POD GURAD varieties where TILLING has been deployed only in the BASF canola breeding program ( Laga et al., 2008 ).…”

TCP Transcription Factors in Pineapple: Genome-Wide Characterization and Expression Profile Analysis during Flower and Fruit Development

“…TCP transcription factors could regulate many biological processes, such as flower development, fruit development, leaf development, and plant hormone signal transduction [13][14][15][16][17][18][19][20][21][22][23][24]. Some TCP members are regulated by microRNA319 [25][26][27][28]. TCP proteins regulate flower development.…”