Advances in research on floral meristem determinacy mechanisms in plants

In higher plants, plant tissues and organs are generated from meristems. Shoot apical meristem (SAM) gives rise to all of the aboveground parts for the entire life of plant through continuous production of new organ primordial, including floral meristem (FM) which finally develops as flowers. Floral development is based on the balance between FM meristem maintenance and termination. At the initial stage, floral stem cells proliferate and produce defined number of floral organs based on the "ABC model" rules. At this stage, FM activity is maintained mainly by CLV (CLAVATA)-WUSCHEL (WUS) feedback loop. WUS encodes a homeodomain containing protein. It promotes stem cell marker gene CLV3 expression when WUS expression is low. It also inhibits CLV3 expression when WUS expression is high. Thus FM activity is maintained and can promote initiation of floral organs. However, after two carpels primordia initiation, FM activity is terminated in a process called FM determinacy. FM determinacy is a dynamic and multi-step process in which WUS plays a central role. WUS expression is regulated by many transcription factors related to floral organ identityAGAMOUS (AG), APETALA2 (AP2) and SUPERMAN, environmental signals (light, temperature, etc.), plant hormones (auxin, cytokinin, gibberellin, etc.) and epigenetic-related factors (histone modification, chromatin remodeling, non-coding RNA, DNA methylation, etc.). Using model plant Arabidopsis, our study noted that AG terminates FM maintenance by directly repressing WUS through chromatin higher structure (chromatin loop), formed by AG and one of Polycomb Group components TERMINAL FLOWER2/LIKE HETEROCHROMATIN PROTEIN1 (TFL2/LHP1); binding to WUS5'-TSS (transcription start site) and WUS3'-CRE (cis-regulatory element). DNA TOPOISOMERASE 1 (TOP1α) inhibited WUS expression by modulating WUS nucleosome density to inhibit DNA accessibility, which also participated in the progress. AUXIN RESPONSE FACTOR3 (ARF3) induced by auxin regulated FM determinacy by repressing cytokinin biosynthesisinhibiting cytokinin synthesis genes ISOPENTENYLTRANSFERASE (IPTs) and LONELY GUY (LOGs) and signalinginhibiting cytokinin receptor gene ARABIDOPSIS HISTIDINE KINASE4 (AHK4), which clarified how auxin and cytokinin integrated to regulate FM activity; FAR-RED ELONGATED HYPOCOTYL 3(FHY3) activated SEPALLATA2, but inhibited CLAVATA3 to regulate meristem determinacy and maintenance, which shed light on how light affected meristem activity. As 3D (3-dimentional) genome organization technology developed, the importance of the impact of chromatin structure on gene expression was realized and more techniques were developed and improved. Using the newly reported methods, FM determinacy mechanism required further in-depth studies. What was more was that since plant FM determinacy was regulated precisely and accurately, any defects in FM determinacy affected seed development. Exploitation of FM determinacy mechanism had the potential to importantly contribute to agricultural production, which was helpful for ensuring reproductive success, seed development and yield of agricultural crops (maize, tomato, etc.). In this review, we gave a short introduction on floral organ identity in Arabidopsis thaliana and the mechanism of meristem maintenance and differentiation. Then we mainly focused on FM determinacy, including some recent studies by our group. Finally, we advanced the application of fundamental studies in crop yields and further prospects for research.