Flowering also has to end: knowns and unknowns of reproductive arrest in monocarpic plants

Abstract

All flowering plants adjust their reproductive period for successful reproduction. Flower initiation is controlled by a myriad of intensively studied factors, so it can occur in the most favorable conditions. However, the end of flowering is also a controlled process, required to optimize the size of the offspring and to maximize resource allocation. Reproductive arrest was described and mainly studied in the last century by physiological approaches, but it is much less understood at the genetic or molecular level. In this review, we present an overview of recent progress in this topic, fueled by highly complementary studies that are beginning to provide an integrated view of how the end of flowering is regulated. In this emerging picture, we also highlight key missing aspects that will guide future research and may provide new biotechnological avenues to improve crop yield in annual plants.

Keywords: APETALA2; FRUITFULL; auxin; cytokinin; death hormone; end of flowering; inflorescence meristem; meristem arrest; proliferative arrest.

Fig. 1.

Morphology of the inflorescence apex in Arabidopsis plants actively proliferating (flowering), arrested (at the end of flowering), or reactivated by pruning of developed fruits after arrest. Cartoons below show the overall aspect of the plants, while in the circled areas, pictures of inflorescences apexes are shown. Note the cluster of unopened buds in arrested inflorescences, in contrast to the developing fruits in basal positions of the stem. In reactivated inflorescences, at least some of these buds do not develop further, and new flowers arise from the reactivated meristem.

Fig. 2.

Summary of factors influencing proliferative arrest. Environmental factors affect the timing of the beginning and the end of flowering, partly through FT, although their precise contribution to proliferative arrest is still largely uncharacterized. Endogenous clues such as age or, more importantly, the production of seeds are major players in the control of the process. In inflorescences in the proliferative state, at earlier stages of the reproductive phase, CK signaling and transcription factors maintaining the activity of the meristem (AP2, WUS) are active, while age-related factors such as miR172 or FUL, negative regulators of AP2, are present at relatively low levels. At the end of the flowering phase, corresponding to the proliferative decline described by Merelo et al. (2022), CK signaling, AP2 and WUS levels decrease, in part by the negative regulation exerted by FUL and miR172, which accumulate with age. WUS decline is accompanied by the cessation of meristem activity, and in the shutdown phase (inflorescence arrest) WUS is no longer detected. In addition, the decreasing levels of AP2 cause high ABA and JA signaling, inducing a dormant-like state of the meristem. Auxin exported from fruits has a strong influence on meristem activity, and it has been proposed that they act to promote the floral arrest phase (Walker et al., 2023).