Gibberellins Act Downstream of Arabis PERPETUAL FLOWERING1 to Accelerate Floral Induction during Vernalization

Abstract

Regulation of flowering by endogenous and environmental signals ensures that reproduction occurs under optimal conditions to maximize reproductive success. Involvement of the growth regulator gibberellin (GA) in the control of flowering by environmental cues varies among species. Arabis alpina Pajares, a model perennial member of the Brassicaceae, only undergoes floral induction during vernalization, allowing definition of the role of GA specifically in this process. The transcription factor PERPETUAL FLOWERING1 (PEP1) represses flowering until its mRNA levels are reduced during vernalization. Genome-wide analyses of PEP1 targets identified genes involved in GA metabolism and signaling, and many of the binding sites in these genes were specific to the A. alpina lineage. Here, we show that the pep1 mutant exhibits an elongated-stem phenotype, similar to that caused by treatment with exogenous GA, consistent with PEP1 repressing GA responses. Moreover, in comparison with the wild type, the pep1 mutant contains higher GA 4 levels and is more sensitive to GA prior to vernalization. Upon exposure to cold temperatures, GA levels fall to low levels in the pep1 mutant and in wild-type plants, but GA still promotes floral induction and the transcription of floral meristem identity genes during vernalization. Reducing GA levels strongly impairs flowering and inflorescence development in response to short vernalization treatments, but longer treatments overcome the requirement for GA. Thus, GA accelerates the floral transition during vernalization in A. alpina, the down-regulation of PEP1 likely increases GA sensitivity, and GA responses contribute to determining the length of vernalization required for flowering and reproduction.

Unraveling the role of MADS transcription factor complexes in apple tree dormancy using sequential DAP-seq

“…The occurrences of predicted motifs were extracted from the corresponding FIMO output produced by the MEME-ChIP suite. Complementally, a custom C++ code was written to manually search the peaks for the presence of a previously described degenerated CArG-box motif, MYHWAWWWRGWWW [89,115].…”

The Diverse Roles of FLOWERING LOCUS C in Annual and Perennial Brassicaceae Species

“…For plants to flower, however, exposure to a minimum of 12 weeks of vernalization is required as inflorescence meristems should develop further during vernalization ( Wang et al, 2009 ; Lazaro et al, 2018 ). The molecular mechanisms enabling floral development during vernalization involve the floral integrator AaSPL15 and increased sensitivity to the growth regulator gibberellin (GA) ( Hyun et al, 2019 ; Tilmes et al, 2019 ). PEP1 expression is still not stably silenced after 12 weeks of vernalization, which leads to floral reversion phenotypes, such as the presence of bracts or flower to inflorescence reversion ( Wang et al, 2009 ; Lazaro et al, 2018 ).…”

Gene regulatory networks controlled by FLOWERING LOCUS C that confer variation in seasonal flowering and life history

“…However, overall, only 14% of binding sites were conserved. In addition, FLC and PEP1 also regulate common pathways related to GA and cold response, but mostly by binding to different genes, and many of these binding sites were specific to the A. alpina lineage, suggesting that the regulation of these pathways has been evolutionarily recruited independently following speciation and might represent convergent evolution ( Mateos et al , 2017 ; Tilmes et al , 2019 ). The involvement of FLC in regulating GA responses was also supported by demonstration of an in vivo interaction between the C-terminus of the MADS domain of FLC and the N-terminal leucine heptad repeat I (LHRI) domain of DELLA proteins such as RGA in Arabidopsis ( Li et al , 2016 ).…”

“…DELLA proteins also interact with SPL9 ( Yu et al , 2012 ; Yamaguchi et al , 2014 ), suggesting that the regulation of the activity of SPL transcription factors by GA during reproductive development is more prevalent ( Zhang et al , 2007 ). It is relevant that FLC and its orthologue in A. alpina , PEP1, directly bind to several genes that encode enzymes required for GA biosynthesis or for GA signalling ( Deng et al , 2011 ; Mateos et al , 2015 ; Tilmes et al , 2019 ). The transcription of some of these genes also increases during vernalization ( Tilmes et al , 2019 ).…”

“…It is relevant that FLC and its orthologue in A. alpina , PEP1, directly bind to several genes that encode enzymes required for GA biosynthesis or for GA signalling ( Deng et al , 2011 ; Mateos et al , 2015 ; Tilmes et al , 2019 ). The transcription of some of these genes also increases during vernalization ( Tilmes et al , 2019 ). This observation suggests that FLC ensures that SPL15 is inactive prior to vernalization by effectively regulating its expression via a feed-forward loop: first, FLC binds directly to the SPL15 promoter to repress its transcription; and, secondly, FLC reduces GA biosynthesis, which increases the level of DELLA proteins that inhibit SPL15 activity.…”