Undoing the ‘nasty: dissecting touch-sensitive stigma movement (thigmonasty) and its loss in self-pollinating monkeyflowers

Abstract

Rapid touch-sensitive stigma closure is a novel plant reproductive trait found in hundreds of Lamiales species. The origins, mechanisms, and functions of stigma closure remain poorly understood, but its repeated loss in self-fertilizing taxa and direct tests implicate adaptive roles in animal-mediated cross-pollination. Here, we document several additional losses of stigma closure in monkeyflowers (Mimulus), then use quantitative trait locus (QTL) mapping and gene expression analyses to provide a first glimpse into the genetic and molecular basis of stigma mechanosensing and movement. Variation in stigma closure in hybrids between selfer/non-closer Mimulus nasutus and outcrosser/fast-closer M. guttatus has a moderately complex genetic basis, with four QTLs together explaining ~70% of parental divergence. Loss of stigma closure in M. nasutus appears genetically independent from other aspects of the floral selfing syndrome and from a parallel loss in M. parishii. Analyses of stylar gene expression in closer M. guttatus, M. nasutus, and a rare M. guttatus non-closer genotype identify functional candidates involved in mechanosensing, turgor regulation, and cell wall remodeling. Together, these analyses reveal a polygenic genetic architecture underlying gain and loss of a novel plant movement, illuminate selfer-outcrosser reproductive divergence, and initiate mechanistic investigations of an unusually visible manifestation of plant intelligence.