Coordinated regulation of vegetative and reproductive branching in rice

Abstract

Grasses produce tiller and panicle branching at vegetative and reproductive stages; the branching patterns largely define the diversity of grasses and constitute a major determinant for grain yield of many cereals. Here we show that a spatiotemporally coordinated gene network consisting of the MicroRNA 156 (miR156/)miR529/ SQUAMOSA PROMOTER BINDING PROTEIN LIKE (SPL) and miR172/ APETALA2 (AP2) pathways regulates tiller and panicle branching in rice. SPL genes negatively control tillering, but positively regulate inflorescence meristem and spikelet transition. Underproduction or overproduction of SPLs reduces panicle branching, but by distinct mechanisms: miR156 and miR529 fine-tune the SPL levels for optimal panicle size. miR172 regulates spikelet transition by targeting AP2-like genes, which does not affect tillering, and the AP2-like proteins play the roles by interacting with TOPLESS-related proteins (TPRs). SPLs modulate panicle branching by directly regulating the miR172/ AP2 and PANICLE PHYTOMER2 (PAP2)/Rice TFL1/CEN homolog 1 (RCN1) pathways and also by integrating other regulators, most of which are not involved in tillering regulation. These findings may also have significant implications for understanding branching regulation of other grasses and for application in rice genetic improvement.he architecture of grasses is largely determined by the branching patterns. Tillers and inflorescence branches are produced at vegetative and reproductive stages, respectively, and their patterns greatly contribute to the diversity of grasses and constitute a major determinant of grain yield of major cereals.Rice branching has attracted much attention because of its importance in food production. Axillary buds produce tillers during the vegetative stage. However, only the early ones formed from the unelongated internodes outgrow as tillers, whereas later ones formed from the upper internodes remain dormant. After reproductive transition, the shoot apical meristem is converted to inflorescence meristem to produce panicle. Rice panicle morphology is largely determined by the timing of identity transition among the different types of meristems (SI Appendix, Fig. S1). Therefore, fine-tuning of meristem phase change at reproductive stage defines the size and architecture of the rice panicle (1).Many genes have been identified as regulators of rice branching. Generally, genes involved in axillary bud initiation control both vegetative and reproductive branching, whereas genes under axillary bud outgrowth have specific roles only at certain stages (2, 3). LAX PANICLE 1 (LAX1) and MONOCULM1 control axillary bud initiation; mutation in either of them results in reduction of both tiller and panicle branches (4, 5). Other genes such as Grain number, plant height, and heading date7 exclusively control panicle branching (6). As a third class, many genes, including Ideal Plant Architecture 1 (IPA1)/Wealthy Farmer's Panicle (WFP) and genes related to strigolactone, play opposite roles in tiller and panicle branches (7-9). Therefore...

Transcriptome Profiling of Wheat Inflorescence Development from Spikelet Initiation to Floral Patterning Identified Stage-Specific Regulatory Genes

“…These genes are involved in panicle branching, flowering time determination, and floral meristem specification in Arabidopsis and rice (Liu et al, 2013b;Teo et al, 2014). Meanwhile, homologs of the SPL7, SPL14, and SPL17 genes that are involved in rice reproductive shoot architecture and grain number determination (Xie et al, 2006;Jiao et al, 2010;Miura et al, 2010;Wang et al, 2015;Liu et al, 2016) also displayed DR-specific expression patterns, suggesting similar roles for these genes in wheat. Such a notion was supported by the in situ hybridization assay, where TaSPL14 was found to be highly expressed in the wheat leaf and bract primordia, and subsequently repressed along the development of the young spike (Fig.…”

“…In wheat (Triticum aestivum), the Q gene, which confers the freethreshing domestication trait, is a close homolog of the maize and rice IDS genes ZmIDS1/OsIDS1 , while wheat FRIZZY PANICLE controls the number of spikelets produced (Dobrovolskaya et al, 2015). Moreover, AP2 transcripts are targets of microRNA 172 (miR172), providing another layer of regulation in spike and floret development (Chuck et al, 2007;Nair et al, 2010;Zhu and Helliwell, 2011;Wang et al, 2015). In Arabidopsis, additional miRNAs, such as miR159, miR167, and miR319, interactively target important TFs that function in meristems to regulate floral organogenesis, such as v-myb avian myeloblastosis viral oncogene homolog (MYBs), Teosinte Branched1/Cycloidea/Proliferating cell factors (TCPs), and auxin response factors (ARFs) (Millar and Gubler, 2005;Wu and Poethig, 2006;Rubio-Somoza and Weigel, 2013;Schommer et al, 2014;Hong and Jackson, 2015;Teotia and Tang, 2015).…”

IPA1: a direct target of SL signaling

“…Consistent with this, overexpressing miR156 results in reduced expression of IPA1 and increased shoot branching, while reducing miR156 expression has opposing effects [9]. It is likely that not all the shoot branching effects of OsmiR156 are mediated by IPA1 because OsmiR156 overexpression lines respond to SL [10], whereas ipa1 lines do not.…”

“…It is likely that not all the shoot branching effects of OsmiR156 are mediated by IPA1 because OsmiR156 overexpression lines respond to SL [10], whereas ipa1 lines do not. The IPA1-independent effects of miR156 on shoot branching may be mediated by other SPLs such as OsSPL7 and OsSPL17 whose mutants also display altered shoot branching phenotypes [9].…”

Identification of MicroRNA Targets of Capsicum spp. Using MiRTrans—a Trans-Omics Approach

“…The miR156 family targeted SBP proteins and played a critical role in regulating phase change and floral induction (Kasschau et al, 2003; Chen et al, 2004; Vazquez et al, 2004; Allen et al, 2005; Wu and Poethig, 2006; Addo-Quaye et al, 2008; Wu et al, 2009). Previous studies reported that miR172 bound to a set of AP2 transcription factors (Addo-Quaye et al, 2008; Li et al, 2010; Song et al, 2011; Lee et al, 2014; Liu et al, 2014; Wang et al, 2014) (Table S9), but presented a variety of functions in different plants: Controlled genes related to flowering time and floral organ in Arabidopsis (Aukerman and Sakai, 2003; Kasschau et al, 2003; Jung et al, 2007; Mathieu et al, 2009; Wang et al, 2009; Wu et al, 2009); regulated inflorescence development in maize (Chuck et al, 2007a,b); involved in the regulation of vegetative and reproductive branching in rice (Zhu et al, 2009; Lee et al, 2014; Wang et al, 2015). The shared miRNA targets among Arabidopsis , maize, rice, and pepper suggested the existence of a similar mechanism of phase change and flowering time control.…”