The Gibberellin perception system evolved to regulate a pre-existing GAMYB-mediated system during land plant evolution

Abstract

Gibberellin (GA) controls pollen development in flowering plants via the GAMYB transcription factor. Here we show that GAMYB is conserved in Selaginella moellendorffii (lycophyte) and Physcomitrella patens (moss), although the former contains the GA signalling pathway, the latter does not. In the lycophyte, GA treatment promotes the outer wall development on microspores, whereas treatment with GA biosynthesis inhibitors disturbs its development. Contrary, in the moss, GAMYB homologue knockouts also produce abnormal spores that resemble Selaginella microspores treated with GA biosynthesis inhibitors and pollen grains of rice gamyb mutant. Moreover, the knockouts fail to develop male organs, instead ectopically forming female organs. Thus, before the establishment of the GA signalling pathway, basal land plants, including mosses, contained a GAMYB-based system for spore and sexual organ development. Subsequently, during the evolution from mosses to basal vascular plants including lycophytes, GA signalling might have merged to regulate this pre-existing GAMYB-based system.Peer reviewe

Genetic and Biochemical Mechanisms of Pollen Wall Development

“…GAMYB, an important component in gibberellin (GA) signaling, regulates pollen wall development by activating the expression of CYP703A3 [81]. Notably, the function of AtMYB103/MYB80 in tapetal and pollen development is conserved among land plants [82,83], as is the regulation of CYP703A3 by GAMYB [84]. In addition, Arabidopsis DYSFUNCTIONAL TAPETUM 1 (DYT1) [85], Defective in Tapetal Development and Function 1 (TDF1) [86], AMS, AtMYB103/MYB80/MS188, and MS1 form a genetic pathway that regulates pollen wall development [87].…”

“…AUXIN RESPONSE FACTOR 17 (ARF17) controls callose biosynthesis and primexine deposition by directly modulating the expression of CalS5 and RPG1 [102]. In flowering plants, GA regulates pollen wall development via GAMYB [81,84], and GAMYB activates targets such as CYP703A3 [81], and the double mutant rga-28 gai-td1, which is defective in the key GA signaling repressor DELLA proteins, displays defective pollen wall development [103]. Cytokinin receptors in the sporophyte are indispensable for pollen maturation [104], and loss of function of ROCK1 (REPRESSOR OF CYTOKININ DEFICIENCY 1) enhances cytokinin response and induces defective exine formation [67].…”

Lycopodium Spores: A Naturally Manufactured, Superrobust Biomaterial for Drug Delivery

“…[ 1,2 ] Such natural packaging means are effective in protecting sensitive biological materials from environmental extremes in the form of prolonged desiccation, UV exposure, and predatory organisms. [ 3 ] A range of plants produce spores as a form of seed, which contains all the genetic material necessary to produce a new plant.…”

Gibberellin Induces Diploid Pollen Formation by Interfering with Meiotic Cytokinesis

“…Although the role of GA in regulating male gametophyte development and maintaining plant male fertility has been widely investigated, our data further clarify that a restriction of GA signaling and associated maintenance of DELLA activity in Arabidopsis is critical for successful male meiotic cell division and gametophytic ploidy stability. The GAMYB transcription factor family is conserved in land plants and seems to regulate a range of reproductive processes (Aya et al, 2011). In agreement with GA being involved in the control of tapetum and microspore development, several members of the GAMYB transcription factor family (MYB33 and MYB65 in Arabidopsis, HvGAMYB in barley, and OSGAMYB in rice) have been shown to be expressed in young anthers prior to flower anthesis (Kaneko et al, 2003;Murray et al, 2003;Millar and Gubler, 2005).…”

“…In rice, for example, impaired GA signaling causes alterations in tapetal cell programmed cell death (Aya et al, 2009), a process that is vital for microspore development through the supplementation of nutrients, hence causing major gametophytic defects such as spore abortion and male sterility. A conserved family of transcription factors, GAMYBs, that are controlled by the GA signaling pathway have been linked with tapetum functioning and pollen outer cell wall formation (Aya et al, 2011). The GAMYB members MYB33 and MYB65 are redundantly required for the development and persistence of the tapetum cell layer during male reproductive development (Millar and Gubler, 2005;Plackett et al, 2011).…”