When growing tall is not an option: contrasting shade avoidance responses in two wild Geranium species

Abstract

Plants can deal with shade in different ways. Sun-adapted species express a set of growth traits to reach for light; the so-called shade avoidance syndrome (SAS). However, shade-tolerant species from the forest understory are not able to outgrow surrounding trees and adopt a tolerance strategy including suppression of shade avoidance. All plants sense the drop in the ratio between red (R) and far-red (FR) light via specialized photoreceptors, the phytochromes, but unlike the molecular pathways promoting SAS, virtually nothing is known about the regulation of shade tolerance. We selected two wild Geranium species with opposite growth responses to FR light enrichment; the shade avoiding G. pyrenaicum and shade tolerant G. robertianum. RNA sequencing of these species revealed contrasting transcriptomic changes treated upon FR light and in the first place showed how differential regulation of phytohormone synthesis and –perception could correlate to the species growth patterns in shade. Analysis of the hormone levels and growth responses to auxin, gibberellic acid and brassinosteroid application or –inhibition confirmed a role for these hormones in the Geranium shade responses. Secondly, the transcriptome analysis revealed a striking difference in FR induced regulation of pathogen defences. G. pyrenaicum showed far-red-mediated down-regulation of defence genes and increased susceptibility to the fungal pathogen Botrytis cinerea, similar to model species Arabidopsis. Interestingly, G. robertianum seems to boost its defences and becomes more resistant when exposed to FR-enriched light. Furthermore, the RNAseq analysis identified genes of which the expression patterns match growth data and give an insight into novel possible players and pathways responsible for the opposite light responses; two receptor-like kinases and a bHLH transcription factor. The importance of these novel candidates was verified in heterologous functional studies in Arabidopsis.