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

Abstract

AbstractRapid 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-closerMimulus nasutusand outcrosser/fast-closerM. guttatushas a moderately complex genetic basis, with four QTLs together explaining ∼70% of parental divergence.Loss of stigma closure inM. nasutusappears genetically independent from other aspects of the floral selfing syndrome and from a parallel loss in M. parishii. Analyses of stylar gene expression in closerM. guttatus,M. nasutus, and a rareM. guttatusnon-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.