INVESTIGATION OF ARABIDOPSIS TSO1, A REGULATOR OF CELL PROLIFERATION AND DIFFERENTIATION

Abstract

Multicellular eukaryotic organisms build complex body structures from a single cell. Through coordinated cell proliferation and differentiation, the collective behavior of cells forms organs that achieve physiological functions. Underlying the developmental processes are the molecular machineries that integrate cell cycle regulation with cell fate acquisition. While animal organogenesis occurs early during embryogenesis, plants maintain pluripotent stem cells at the growing tips (meristems) and generate organs iteratively throughout lifespan. The amazing ability to balance stem cell self-renewal and differentiation underlies the extreme longevity of some plants species. Despite the differences, common mechanisms exist across plant and animal developmental regulation. Understanding both unique and common mechanisms of plant development has broad implications on basic science as well as agriculture and medicine.

The Arabidopsis TSO1 gene is a regulator of cell proliferation and differentiation at the shoot and root meristems. TSO1 encodes a CXC domain protein and its animal homologs encode core components of a cell cycle regulatory complex, the DREAM complex. To investigate TSO1 function and identify factors that act together with TSO1, I carried out two genetic screens for suppressors and enhancers of tso1 mutants. I discovered that loss-of-function mutations in MYB3R1, which encodes the Arabidopsis ortholog of human B-Myb, can suppress tso1 mutant defects at both the shoot and root meristems. In tso1-1 mutant, MYB3R1 is over and ectopically expressed at the shoot and root meristems. Furthermore, MYB3R1 phospho mimic enhanced the tso1-3 phenotype, indicating that hyper-active MYB3R1 may mediate the tso1-1 phenotype. TSO1 physically interacts with MYB3R1 and likely forms a plant DREAM-like complex that operates in the plant meristems to balance cell proliferation with differentiation.

A gain-of-function mutation of a HD-ZIP III transcription factor, REVOLUTA (REV), was identified as an enhancer of tso1 mutants. TSO1 directly represses REV transcription to balance adaxial and abaxial polarity of lateral organs and maintains the shoot apical meristem. This genetic and molecular interaction between TSO1 and the adaxial factor REV presents an integration point of cell cycle, lateral organ polarity, and meristem regulation.

Together, our findings demonstrate a cell cycle regulatory module conserved across plants and animals and describe its integration into plant specific developmental context.