Photocontrol of Axillary Bud Outgrowth by MicroRNAs: Current State-of-the-Art and Novel Perspectives Gained From the Rosebush Model

Abstract

Shoot branching is highly dependent on environmental factors. While many species show some light dependence for branching, the rosebush shows a strict requirement for light to allow branching, making this species an excellent model to further understand how light impinges on branching. Here, in the first part, we provide a review of the current understanding of how light may modulate the complex regulatory network of endogenous factors like hormones (SL, IAA, CK, GA, and ABA), nutrients (sugar and nitrogen), and ROS to control branching. We review the regulatory contribution of microRNAs (miRNAs) to branching in different species, highlighting the action of such evolutionarily conserved factors. We underline some possible pathways by which light may modulate miRNA-dependent regulation of branching. In the second part, we exploit the strict light dependence of rosebush for branching to identify putative miRNAs that could contribute to the photocontrol of branching. For this, we first performed a profiling of the miRNAs expressed in early light-induced rosebush buds and next tested whether they were predicted to target recognized regulators of branching. Thus, we identified seven miRNAs (miR156, miR159, miR164, miR166, miR399, miR477, and miR8175) that could target nine genes (CKX1/6, EXPA3, MAX4, CYCD3;1, SUSY, 6PFK, APX1, and RBOHB1). Because these genes are affecting branching through different hormonal or metabolic pathways and because expression of some of these genes is photoregulated, our bioinformatic analysis suggests that miRNAs may trigger a rearrangement of the regulatory network to modulate branching in response to light environment.

Keywords: branching; lateral meristem; light control; post-transcriptional regulation; rose; small RNAs.

FIGURE 1

Network of main actors controlling axillary bud outgrowth in the rosebush Rosa ‘Radrazz’* and the potential targets of miRNAs based on literature in other plant species** Potential gene targets of these miRNAs in the control of bud outgrowth are represented in dotted orange circles. miRNAs involved in control of bud outgrowth according to the literature are represented in orange. Blue represents hormonal pathway, green sugars pathway, purple ROS pathway. Arrows head means induction, straight lines mean repression, white lightning bolt means induction by light, darked lightning bolts means induction by darkness. *Girault et al. (2008), Girault et al. (2010), Henry et al. (2011), Choubane et al. (2012), Rabot et al. (2012), Rabot et al. (2014), Djennane et al. (2014), Barbier et al. (2015), Roman et al. (2016), Roman et al. (2017), Porcher et al. (2020), Porcher et al. (2021), Wang M. et al. (2021). **Jiao et al. (2010), Miura et al. (2010), Wang et al. (2010), Wei et al. (2012), Xia et al. (2012), Curaba et al. (2013), Zhou et al. (2013), Zhang et al. (2013), Aung et al. (2015), Wang L. et al. (2015), Wang Y. et al. (2015), Huang et al. (2017), Kravchik et al. (2019), Sun et al. (2019), Cui et al. (2020), Lian et al. (2021), Wang R. et al. (2021), Zhan et al. (2021).

FIGURE 2

Potential role of miRNAs in the control of axillary bud outgrowth and their light regulation in plants. In bright blue miRNAs identified in the present study as putative novel regulators in control of bud outgrowth. Black arrows heads mean induction, straight lines mean repression, white lightning bolt means induction by light, darked lightning bolt means induction by darkness, red cross means repression of the miRNA.