Unlike animals, all land plants have a haploid gametophyte stage of their life cycle. Gametophytes are multicellular plants that contain one half the chromosome complement of the diploid phase, the sporophyte. In bryophytes like mosses, the gametophyte is dominant, while in familiar angiosperms like maize the diploid sporophyte dominates. In all cases, development of above ground structures depends upon the activity of apical meristems, pools of self-propagating stem cells located at the growing plant tips. Widespread variation in meristem structure has evolved across these wide groups; despite this structural variation, meristem function during organogenesis and stem cell renewal is conserved. Major evolutionary innovations in shoot development include the dominance of the sporophyte generation over the gametophyte, and the emergence of multicellular shoot apical meristems that produce photosynthetic leaves. In this project, analyses of gene expression networks in plant shoot apices will identify shared and unique mechanisms for apical meristematic development among the ancient gametophyte-dominant model bryophytes Marchantia polymorpha and Physcomitrella patens, and the recently evolved sporophyte-dominant angiosperms Zea mays and Arabidopsis thaliana. Laser-microdissection coupled with RNA-sequencing will compare shoot apical transcriptomic signatures from these diverse model plants. Three categories of candidate gene will be identified: (1) functionally shared transcripts among the gametophyte meristems or lateral organs of the bryophytes and the sporophyte meristem or lateral organ of maize and Arabidopsis; (2) sporophyte-specific transcripts among the four model organisms, and; (3) transcripts unique to each lineage and domain. All data generated during this project will be released to public databases, including the TRANSCRIPTOME link at the CosMoss database for Physcomitrella patens, and the Marchantia polymorpha database at the DOE Joint Genome Institute. This project also will provide training in genomic analyses and mechanisms of plant development for a Cornell University Plant Biology graduate student.
Unlike animals, all land plants form haploid gametophytes, multicellular organisms that contain one half the chromosome complement of the diploid parental plant (sporophyte). Development of all above ground (shoot) structures in the plant is dependent upon the activity of apical meristems, pools of self-propagating stem cells located at the growing tips of plants. Widespread variations in shoot meristem structure have evolved among living plant lineages. Examples include the single-celled apices of the non-vascular bryophytes, the multicellular meristems with prominent apical cells in the seedless lycophytes, and the multiple cell-layered shoot meristems of flowering plants (angiosperms). Despite this variation in shoot apical structure, meristem function during organogenesis and stem cell renewal is conserved throughout plant evolution. Major innovations during the evolution of plant shoot development include the dominance of the sporophyte generation over the gametophyte, the emergence of multicellular shoot apical meristems that produce photosynthetic leaves, and lateral meristems that enable branching. In this project, analyses of gene expression networks in plant shoot apices identified shared and unique mechanisms for apical meristematic development among the ancient gametophyte-dominant model organisms Marchantia and Physcomitrella, and the recently evolved sporophyte-dominant angiosperm Zea mays. In this project, we used laser-microdissection coupled with RNA-sequencing to compare transcriptomic signatures from the sporophytes and discrete apical meristem domains in the gametophytes of two model bryophytes (the moss Physcomitrella patens and the liverwort Marcantia polymorpha), with apical meristem domains from the sporophyte-dominant angiosperm Zea mays (maize). Three categories of candidate genes implicated in meristem evolution were identified: (1) functionally shared transcripts among the gametophyte meristems or lateral organs of the bryophytes and the sporophyte meristem or lateral organ of maize (2) sporophyte-specific transcripts among the four model organisms and; (3) transcripts unique to each lineage and domain. These experiments broadly address three fundamental questions surrounding the evolution of developmental mechanisms during land plant evolution, including: (1) What is the molecular basis for the shift from a gametophyte-dominant to a sporophyte-dominant life cycle? (2) What are the shared molecular genetic networks that describe a functional apical meristem in the gametophytes of model bryophytes and the sporophyte of a model vascular plant? (3) What are the unique developmental genetic pathways that have separately evolved gametophyte-dominant and in sporophyte-dominant plants? The data show that there are >700 differentially expressed gene families shared across the Maize SAM, Moss, and Marchantia sporophytes. Notably, several (614) maize meristem patterning gene families that are missing from the Marchantia sporophyte are found in the moss sporophyte. Thus, Moss sporophytes express key meristem patterning gene families that are not found in Marchantia sporophytes. We speculate that this transcriptomic data may reflect the fact that the Moss sporophyte and the Maize SAM both exhibit patterned and asymmetric apical cell divisions, whereas in Marchantia the sporophyte divides symmetrically throughout. Significantly, fewer than 250 differentially expressed gene families are found in common in the Maize SAM and the bryophyte (Moss and Marcantia) gametophyte apices (meristems). Thus, Maize and bryophyte meristems share some key meristem genes – however, significant meristem regulators are missing. Moreover, the Moss gametophyte meristem, which makes successive leaflike organs in a phyllotactic pattern much like maize, shares a total of 1383 gene families with maize. In contrast the Marcantia gametophyte apex, which does not reiteratively form leaflike organs but forms a continuously growing appendage called a thallus, shares only 282 gene families with the Maize SAM. These data are in agreement with morphological data suggesting that Maize SAM function is more similar to that of moss gametophytic apical meristem function than it is to liverwort apical function Taken together, the data reveal that the maize SAM displays gene expression patterns that are shared with both the moss gametophyte and the sporophyte.