Analyses Of Structure-Function Relationships In The Evolution Of Embryophyte Shoot Meristems: A Transcriptomic Survey
Shoot apical meristems (SAMs) have increased in complexity over the course of embryophyte evolution from single apical initials that generate the gametophytic body plans in bryophytes, to the histologically stratified, multicellular SAMs that give rise to the entire sporophytic shoot in angiosperms. Despite this diversity in shoot apical structure, our understanding of the genes involved in SAM function is largely limited to the angiosperms. In this thesis, I use laser microdissection coupled with RNA-sequencing (LM-RNAseq) to generate domain specific gene expression profiles for meristem cells as well as sporophytic bryophyte embryos. These data were used to address major questions pertaining to transitions in embryophyte evolution. In chapter two I explore the developmental genetic programs that control multidimensionally dividing bud cells versus unidimensionally dividing tip cells in the moss Physcomitrella patens. I identify over 4,000 transcript profiles distinguishing the two stem cell types. Moreover the bud cell transcriptomes have significantly up-regulated programs involving meristem development and asymmetric cell division. From this work I propose a model wherein the merger of these two programs allows the unicellular moss meristem to balance its essential functions of self-maintenance with organogenesis. In chapter three I look into the molecular basis of sporophyte shoot meristem evolution. I ask if angiosperm meristem patterning genes expressed in the sporophytic SAM of Zea mays are expressed in the gametophytic SAM, or in the non-meristematic sporophyte, of the model bryophytes Marchantia polymorpha and Physcomitrella patens. I identify an abundance of up-regulated genes involved in stem cell maintenance and organogenesis in the maize SAM and in both the gametophytic meristem and sporophyte of moss, but not in Marchantia. I use these findings to build a framework for sporophytic meristem evolution involving the concerted selection of ancestral meristem gene programs from gametophyte-dominant lineages. In chapter four I investigate the functional relationships amongst the AC-type meristem structures found in Selaginella and Equisetum and the angiosperm meristem structure found in maize. The analyses indicate that pluripotent cell functions reside within the prominent AC. I also identify homologs for angiosperm SAM maintenance genes across multiple domains in the Equisetum and Sellaginella SAMs, implying that meristem maintenance is not restricted to the prominent AC that defines these SAMs. Moreover, the transcriptional profiles for the two AC-type SAMs are definitively distinct from one another, providing the first molecular support for the convergent evolution of AC-type SAM structures within these vascular plant lineages. The data presented here bring a new awareness to the developmental genetic processes that may have contributed towards pivotal innovations in land plant evolution.
Shoot meristem; Land plant evolution; Transcriptomics
Scanlon, Michael J.
Nasrallah, June Bowman; Niklas, Karl Joseph; Stevenson, Dennis
Ph.D. of Plant Biology
Doctor of Philosophy
dissertation or thesis