Gene regulatory network and abundant genetic variation play critical roles in heading stage of polyploidy wheat

Abstract

Background: The extensive adaptability of polyploidy wheat is attributed to its complex genome, and accurately controlling heading stage is a prime target in wheat breeding process. Wheat heading stage is an essential growth and development processes since it starts at a crucial point in the transition from vegetative phase to reproductive phase.

Main body: Heading stage is mainly decided by vernalization, photoperiod, hormone (like gibberellic acid, GA), and earliness per se (Eps). As a polyploidy species, common wheat possesses the abundant genetic variation, such as allelic variation, copy number variation etc., which have a strong effect on regulation of wheat growth and development. Therefore, understanding genetic manipulation of heading stage is pivotal for controlling the heading stage in wheat. In this review, we summarized the recent advances in the genetic regulatory mechanisms and abundant variation in genetic diversity controlling heading stage in wheat, as well as the interaction mechanism of different signals and the contribution of different genetic variation. We first summarized the genes involved in vernalization, photoperoid and other signals cross-talk with each other to control wheat heading stage, then the abundant genetic variation related to signal components associated with wheat heading stage was also elaborated in detail.

Conclusion: Our knowledge of the regulatory network of wheat heading can be used to adjust the duration of the growth phase for the purpose of acclimatizing to different geographical environments.

Keywords: Gene regulatory network; Genetic variation; Heading stage; Photoperiod; Polyploidy wheat; Vernalization.

Fig. 1

Wheat heading stage are affected by multi-environment. Based on the growth habit of winter wheat, hormone and earliness per se (Eps) can work on the whole life of the wheat growth and development, vernalization always being to take effect on the transition from the vegetative phase to reproductive phase during winter time, following by vernalization, photoperiod functioned to control flowering. Different colors represent different signals

Fig. 2

Schematic summary of the wheat heading stage regulatory network. Before vernalization, VRN2 competes with other CCT-domain proteins (like CO2) to interact with NF-Y transcription factors to inhibit the transcription of VRN3. Secondly, TaGRP2 can directly bind to this binding site of VRN1 to prevent transcript accumulation. Thirdly, TaVRT-2 can directly bind to the CArG box of the TaVRN1 promoter in vivo to inhibit its activity, and this inhibition is enhanced by VRN2. Following vernalization, VRN1 transcripts were enhanced by changing the ratio of H3K4me3 to active gene transcription. However, the expression level of VRN2 decreases after vernalization to release VRN3, then they can move from the leaves to the apices via the phloem. In the stem apical meristem, the VRN3 protein then forms a functional protein complex with TaFDL to bind the CArG box domain in the promoter of VRN1 in vitro, leading to transcriptional activation. Meanwhile, phosphorylated VER2 (VER2-P) transfers into the nucleus and then gathers in the shoot tips and young leaves, physically interacting with the RNA-binding protein TaGRP2, which is O-GlcNAc-modified,to decrease the inhibitory action on VRN1 expression. Furthermore, the expression levels of TaVRT2 and VRN2 decrease, and VRN1 gradually accumulates. Finally, the expression level of VRN1 is significantly enhanced to accelerate flowering. VRN-D4, as a duplicated copy of VRN1, expresses in the leaves and accumulates after prolonged exposure to low temperature, and can directly or indirectly influence VRN1 among the three vernalization genes the earliest, but has less effect than Vrn-A1. Long-day (LD) induces the accumulation of physiologically active Pfr (PHYB:PHYC heterodimers and PHYC:PHYC homodimers) and then activates the transcription of PPD1 and circadian clock output genes CO2/TaDH1, and the VRN3 transcript can be promoted by PPD1 and CO2. However, PPD1 is inhibited by WPCL1, which is a flowering negative regulator, but the interaction mechanism of these two genes is unknown. TaGI, which is controlled by the circadian clock under a light/dark cycle, works on the upstream of CO and produces a bulky protein complex with other suspected proteins, binding to the critical region in the CO gene promoter to induce its transcription. Eps genes work throughout wheat growth and development via an unknown pathway, Green arrows represent promotion, red arrows represent inhibition in the signal pathway