Molecular control of the floral transition in the mast seeding plant Celmisia lyallii (Asteraceae)

Abstract

Mast flowering (or masting) is synchronous, highly variable flowering among years in populations of perennial plants. Despite having widespread consequences for seed consumers, endangered fauna and human health, masting is hard to predict. While observational studies show links to various weather patterns in different plant species, the mechanism(s) underpinning the regulation of masting is still not fully explained. We studied floral induction in Celmisia lyallii (Asteraceae), a mast flowering herbaceous alpine perennial, comparing gene expression in flowering and nonflowering plants. We performed translocation experiments to induce the floral transition in C. lyallii plants followed by both global and targeted expression analysis of flowering‐pathway genes. Differential expression analysis showed elevated expression of ClSOC1 and ClmiR172 (promoters of flowering) in leaves of plants that subsequently flowered, in contrast to elevated expression of ClAFT and ClTOE1 (repressors of flowering) in leaves of plants that did not flower. The warm summer conditions that promoted flowering led to differential regulation of age and hormonal pathway genes, including ClmiR172 and ClGA20ox2, known to repress the expression of floral repressors and permit flowering. Upregulated expression of epigenetic modifiers of floral promoters also suggests that plants may maintain a novel “summer memory” across years to induce flowering. These results provide a basic mechanistic understanding of floral induction in masting plants and evidence of their ability to imprint various environmental cues to synchronize flowering, allowing us to better predict masting events under climate change.

Studying the genetic basis of masting

“…Applying advances in genome-wide transcriptomics (e.g. DNA microarray and RNAseq) [25,64] is also promising to unravel the underlying mechanism of dynamic environmental response of genes and its effect on masting. In fact, a molecular phenology approach that monitors seasonal recurring gene expression patterns in natura [19] has been increasingly used in non-model organisms [21,25,64,65].…”

“…Investigation of these gene families in masting species opens a new direction for the evolution of masting studies, allowing us to elucidate whether species with different life-history strategies and mating systems use similar genetic pathways to produce different phenotypes. Using genomewide transcriptome analysis as a useful first step in describing patterns of gene expression and finding a molecular marker for traits of interest, several studies demonstrated that masting is genetically regulated at the stage of floral transition [22,23,25,64,65]. Monitoring major flowering-time genes (FcFT, FcLFY and FcAP1) in F. crenata Blume (figure 2a) in leaves and buds over 8 years demonstrated that biennial flowering dynamics is caused by on-off cycles in these flowering-time genes (figure 2b), which was highly correlated with fluctuation royalsocietypublishing.org/journal/rstb Phil.…”

“…In the masting alpine daisy Celmisia lyallii, flower initiation was associated with the suppression of TARGET OF EAT1 (TOE1) and ANTI-FT (AFT) and activation of micro-RNA 172 (miR172), leading to increases of the floral integrator SOC1 (figure 3) [25]. Transcriptome analysis of plant samples taken in the summer of floral transition from rosettes that subsequently flowered or remained vegetative revealed a wide range of genes with differential expression, including those associated with tissue maturity (ageing; miR172), warm or There are also possible roles in some plants for epigenetic changes to integrate environmental cues across several months or years [26,69].…”

“…A range of different factors, including tissue age (miR172), temperatures (TOE1, PIF4, AFT, CLF) and resources (TPS1), affect the flowering integrator genes (SOC1 and TFL1) that then trigger flower production. Taken from [25] with permission.…”

“…This new area of research will significantly benefit masting studies because it will contribute to identifying 'masting genes', which are the basis of masting traits. To date, only a few trials have been made to apply recent progress in molecular and genetic studies to masting species [21][22][23][24][25][26].…”