FHY3 and FAR1 Integrate Light Signals with the miR156-SPL Module-Mediated Aging Pathway to Regulate Arabidopsis Flowering

Abstract

In response to competition for light from their neighbors, shade-intolerant plants flower precociously to ensure reproductive success and survival. However, the molecular mechanisms underlying this key developmental switch are not well understood. Here, we show that a pair of Arabidopsis transcription factors essential for phytochrome A signaling, FAR-RED ELONGATED HYPOCOTYL3 (FHY3) and FAR-RED IMPAIRED RESPONSE1 (FAR1), regulate flowering time by integrating environmental light signals with the miR156-SPL module-mediated aging pathway. We found that FHY3 and FAR1 directly interact with three flowering-promoting SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors, SPL3, SPL4, and SPL5, and inhibit their binding to the promoters of several key flowering regulatory genes, including FRUITFUL (FUL), LEAFY (LFY), APETALA1 (AP1), and MIR172C, thus downregulating their transcript levels and delaying flowering. Under simulated shade conditions, levels of SPL3/4/5 proteins increase, whereas levels of FHY3 and FAR1 proteins decline, thus releasing SPL3/4/5 from FHY3/FAR1 inhibition to allow activation of FUL, LFY, AP1, and MIR172C and, consequently, early flowering. Taken together, these results unravel a novel mechanism whereby plants regulate flowering time by integrating environmental cues (such as light conditions) and an internal developmental program (the miR156-SPL module-mediated aging pathway).

The trehalose 6‐phosphate pathway impacts vegetative phase change in Arabidopsis thaliana

“…Transgenic plants overexpressing miR156‐resistant versions of SPL3 , SPL4 , SPL5 , SPL10 , and SPL11 ( rSPL3 , rSPL4 , rSPL5 , rSPL10 , and rSPL11 ), respectively, revealed that SPL3, SPL4, and SPL5 proteins promote the adult phase, including flowering (Cardon et al ., 1999; Wu and Poethig, 2006; Shikata et al ., 2009), whereas SPL10 and SPL11 play only minor roles (Huijser and Schmid, 2011). In agreement with this observation, a spl3 spl4 spl5 triple knockout mutant generated via CRISPR/Cas9 flowered significantly later than Col‐0 plants (Xie et al ., 2020). Based on single and double mutant analyses (Shikata et al ., 2009), SPL2, which belongs to the same phylogenetic clade as SPL10 and SPL11, was proposed to have only a weak effect on vegetative phase change (Riese et al ., 2007).…”

Control of theAzollasymbiosis sexual reproduction: ferns to shed light on the origin of floral regulation?

“…ft mutant Arabidopsis flowered earlier under incandescent light (Martinez-Zapater & Somerville, 1990) or in TL with far-red LED compared to in TL (Schluepmann et al, unpublished) suggesting that FT is not involved. Signaling was also reported via PHYBregulated PIF4 protein complexes that bind the promoters of miRNA156/172 directly with interference from PHYA-regulated TF (Sánchez-Retuerta et al, 2018;Sun et al, 2018;Xie et al, 2020). In the present study, the highly induced MIKC C turned out a paralogue of SOC1, and miR156/172 steady states were unaltered by the far-red triggered transition to RD in A. filiculoides ( Figure 7B; Supplemental Table 6) suggesting that mechanisms in ferns and seed plant RD are not conserved.…”

“…Far-red light responses in Azolla ferns look alike a shade-avoidance syndrome but signal transduction pathways that mediate them in ferns remain largely uncharacterized (Inoue et al, 2017). Pathways causing shade response components are known to use alternative phytochromes and interacting factors (Possart et al, 2013;Xie et al, 2020).…”

“…Moreover, AP2/TOE and NIN TF are known to mediate repression of SOC1 in Arabidopsis on high nitrate (Gras et al, 2018;Olas et al, 2019). The MIKC C SOC1 is further known to control levels of miR319 that inhibits TCP protein functions in the FT-FD complex mediating photoperiod control of RD (Lucero et al, 2017;Li et al, 2020). Inextricably, therefore, transition to RD is linked to conserved miRNA modules in angiosperms but we know little of miRNA loci in ferns (Berruezo et al, 2017;You et al, 2017).…”

Beyond flowering time: diverse roles of an APETALA2‐like transcription factor in shoot architecture and perennial traits

“…Transgenic A. alpina lines with reduced miR156 activity or overexpressing the miR156 ‐resistant form of AaSPL15 , flower when vernalised as young seedlings (grown for 2 or 3 wk before vernalisation) (Bergonzi et al ., 2013; Hyun et al ., 2019). We demonstrated that miR172 accumulation increased when A. alpina plants became older, resembling previous studies in Arabidopsis thaliana and other species, a mechanism regulated by SPL9, SPL10 and SPL3/4/5 (Aukerman & Sakai, 2003; Chuck et al ., 2007; Wu et al ., 2009; Xie et al ., 2020). We also established a role for AaTOE2 in reproductive competence and placed AaSPL5 downstream of AaTOE2 (Fig.…”