In order to maintain global food security, it will be necessary to increase yields of the cereal crops that provide most of the calories and protein for the world's population, which includes common wheat (Triticum aestivum L.). An important wheat yield component is the number of grain-holding spikelets which form on the spike during inflorescence development. Characterizing the gene regulatory networks controlling the timing and rate of inflorescence development will facilitate the selection of natural and induced gene variants that contribute to increased spikelet number and yield. In the current study, co-expression and gene regulatory networks were assembled from a temporal wheat spike transcriptome dataset, revealing the dynamic expression profiles associated with the progression from vegetative meristem to terminal spikelet formation. Consensus co-expression networks revealed enrichment of several transcription factor families at specific developmental stages including the sequential activation of different classes of MIKC-MADS box genes. This gene regulatory network highlighted interactions among a small number of regulatory hub genes active during terminal spikelet formation. Finally, the CLAVATA and WUSCHEL gene families were investigated, revealing potential roles for TtCLE13, TtWOX2, and TtWOX7 in wheat meristem development. The hypotheses generated from these datasets and networks further our understanding of wheat inflorescence development.

Background

Photoperiod signals provide important cues by which plants regulate their growth and development in response to predictable seasonal changes. Phytochromes, a family of red and far-red light receptors, play critical roles in regulating flowering time in response to changing photoperiods. A previous study showed that loss-of-function mutations in either PHYB or PHYC result in large delays in heading time and in the differential regulation of a large number of genes in wheat plants grown in an inductive long day (LD) photoperiod.

Results

We found that under non-inductive short-day (SD) photoperiods, phyB-null and phyC-null mutants were taller, had a reduced number of tillers, longer and wider leaves, and headed later than wild-type (WT) plants. The delay in heading between WT and phy mutants was greater in LD than in SD, confirming the importance of PHYB and PHYC in accelerating heading date in LDs. Both mutants flowered earlier in SD than LD, the inverse response to that of WT plants. In both SD and LD photoperiods, PHYB regulated more genes than PHYC. We identified subsets of differentially expressed and alternatively spliced genes that were specifically regulated by PHYB and PHYC in either SD or LD photoperiods, and a smaller set of genes that were regulated in both photoperiods. We found that photoperiod had a contrasting effect on transcript levels of the flowering promoting genes VRN-A1 and PPD-B1 in phyB and phyC mutants compared to the WT.

Conclusions

Our study confirms the major role of both PHYB and PHYC in flowering promotion in LD conditions. Transcriptome characterization revealed an unexpected reversion of the wheat LD plants into SD plants in the phyB-null and phyC-null mutants and identified flowering genes showing significant interactions between phytochromes and photoperiod that may be involved in this phenomenon. Our RNA-seq data provides insight into light signaling pathways in inductive and non-inductive photoperiods and a set of candidate genes to dissect the underlying developmental regulatory networks in wheat.