Photoperiod-dependent regulation of secondary growth by auxin flux: how it occurs and how to benefit from it

Abstract

Photoperiod is a crucial environmental signal that orchestrates the seasonal growth cycle in temperate forest trees. While its role in regulating primary growth through well characterized molecular pathways like the FLOWERING LOCUS T (FT)/TERMINAL FLOWER1 (TFL1) module is established, the mechanisms governing the photoperiodic control of secondary growth – the process responsible for wood formation and the majority of terrestrial carbon sequestration – remain poorly understood. This review synthesizes current evidence to explore the hypothesis that auxin (indole-3-acetic acid) flux, determined by its biosynthesis, transport, and metabolism, serves as an important mechanism through which photoperiod regulates secondary growth. First, I critically evaluate the role of auxin flux in the photoperiodic control of key xylem developmental stages (cell division, enlargement, and maturation). Second, I dissect the relationship between primary and secondary growth under changing day length, arguing that auxin supply is not a passive consequence of photoperiod-dependent apical growth but is independently regulated. Third, I examine emerging molecular mechanisms that could underlie photoperiod-dependent changes in auxin flux, highlighting an abscisic acid-dependent pathway involving Vascular Cambium-related MADS 1 and 2 (VCM1/2) and PIN-FORMED5b (PIN5b) in poplar, and discussing the potential, yet less-defined, roles of FT/TFL1-like and CIRCADIAN CLOCK ASSOCIATED 1 (CCA1)/LATE ELONGATED HYPOCOTYL (LHY)-like factors. Finally, I discuss the potential of manipulating the photoperiod-auxin flux relationship to enhance late-season growth and drought resilience in trees, proposing a synthetic biology approach to engineer photoperiod-insensitive auxin biosynthesis as a strategy to optimize tree performance under rapidly changing climatic conditions.