Hormonal interactions and gene regulation can link monoecy and environmental plasticity to the evolution of dioecy in plants

• Published in: American journal of botany 2013-06, Vol.100 (6), p.1022-1037
• Main Authors: Golenberg, Edward M, West, Nicholas W
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - genetics; Adaptation, Physiological - physiology; alleles; Auxins; Biological Evolution; Botany; dioecy; environmental sex determination; Evolution; flower development; flowers; Flowers & plants; gender; Gene expression; Genes; genetic sex determination; hermaphroditism; hormone crosstalk; hormone regulation; Hormones; Magnoliophyta; Masculinity; monoecy; mutation; Plant biology; Plant growth regulators; Plant Growth Regulators - genetics; Plant Growth Regulators - metabolism; plant hormones; Plant Physiological Phenomena - genetics; Plants; Plants - genetics; Population genetics; regulatory sequences; Reproduction - genetics; Reproduction - physiology; Sex determination; sex hormones; sexual plasticity; Special Section: Ecological Interactions and the Evolution of Plant Mating Systems; Species; Stress response
• ISSN: 0002-9122; 1537-2197
• DOI: 10.3732/ajb.1200544

Most models for dioecy in flowering plants assume that dioecy arises directly from hermaphroditism through a series of independent feminizing and masculinizing mutations that become chromosomally linked. However, dioecy appears to evolve most frequently through monoecious grades. The major genetic models do not explain the evolution of unisexual flowers in monoecious and submonoecious populations, nor do they account for environmentally induced sexual plasticity. In this review, we explore the roles of environmental stress and hormones on sex determination, and propose a model that can explain the evolution of dioecy through monoecy, and the mechanisms of environmental sex determination.Environmental stresses elicit hormones that allow plants to mediate the negative effects of the stresses. Many of these same hormones are involved in the regulation of floral developmental genes. Recent studies have elucidated the mechanisms whereby these hormones interact and can act as switchpoints in regulatory pathways. Consequently, differential concentrations of plant hormones can regulate whole developmental pathways, providing a mechanism for differential development within isogenic individuals such as seen in monoecious plants. Sex-determining genes in such systems will evolve to generate clusters of coexpressed suites. Coexpression rather than coinheritance of gender-specific genes will define the sexual developmental fate. Therefore, selection for gender type will drive evolution of the regulatory sequences of such genes rather than their synteny. Subsequent mutations to hyper- or hyposensitive alleles within the hormone response pathway can result in segregating dioecious populations. Simultaneously, such developmental systems will remain sensitive to external stimuli that modify hormone responses.