. The long-term goal of this work is to understand the molecular genetic mechanisms that underlie developmental complexity. Multicellularity has evolved multiple times in the history of life and has led to an explosion of eukaryotic diversity, including novel reproductive strategies. Sexual dimorphism and multicellularity have coevolved in several lineages, but the mechanisms that led to their co-evolution in animals and plants lie in the distant past and are unknown. Volvox carteri is a multicellular green alga that shares recent common ancestry with its closest unicellular relative, Chlamydomonas reinhardtii. From a single-celled Chlamydomonas ancestor V. carteri has evolved many metazoan-like features including complete germ-soma separation and sexually dimorphic development. During sexual differentiation V. carteri females produce eggs and males produce sperm, a trait that is controlled by a mating type (mt) locus with two alleles, mtf (female) and mtm (male). The genomic region that encodes V. carteri mt has been identified and partially characterized, leading to the following Aims: (i) Clone and sequence both alleles of mt;(ii) Use annotation and transcriptional profiling to identify key regulators of sex determination;(iii) Characterize the genes that are responsible for sexually dimorphic development including vMATS, a mt-linked retinoblastoma (RB) tumor suppressor homolog that is highly polymorphic between V. carteri males and females;(iv) Directly test the role of female and male vMATS isoforms and other potential sex determining genes in regulating sexual differentiation by using ectopic expression and genetic inactivation experiments. The discovery of the V. carteri mating locus provides an unprecedented opportunity to dissect the molecular genetic changes that underlie the evolution of sexual dimorphism and to understand how sex chromosomes evolve to influence developmental programming.

Public Health Relevance

. Germ cells are critical for human reproductive health and are also associated with some forms of human cancer, but their biology is poorly understood. The work proposed here is expected to reveal the underlying genetic architecture that leads to the production of eggs and sperm in a simple model system, and has already uncovered a potentially conserved link between a human tumor suppressor and germ cell formation.

National Institute of Health (NIH)
National Institute of General Medical Sciences (NIGMS)
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Genetic Variation and Evolution Study Section (GVE)
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Eckstrand, Irene A
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Salk Institute for Biological Studies
La Jolla
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Umen, James; Goodenough, Ursula; Heitman, Joseph (2017) Eukaryotic Sexual Reproduction Evoked ""with a Little Help from My Friends"". Cell 170:1059-1061
Hamaji, Takashi; Lopez, David; Pellegrini, Matteo et al. (2016) Identification and Characterization of a cis-Regulatory Element for Zygotic Gene Expression in Chlamydomonas reinhardtii. G3 (Bethesda) 6:1541-8
Hamaji, Takashi; Mogi, Yuko; Ferris, Patrick J et al. (2016) Sequence of the Gonium pectorale Mating Locus Reveals a Complex and Dynamic History of Changes in Volvocine Algal Mating Haplotypes. G3 (Bethesda) 6:1179-89
Matt, Gavriel; Umen, James (2016) Volvox: A simple algal model for embryogenesis, morphogenesis and cellular differentiation. Dev Biol 419:99-113
Umen, James G (2015) Lost and Found: The Secret Sex Lives of Bdelloid Rotifers. Genetics 200:409-12
Cross, Frederick R; Umen, James G (2015) The Chlamydomonas cell cycle. Plant J 82:370-92
Lopez, David; Hamaji, Takashi; Kropat, Janette et al. (2015) Dynamic Changes in the Transcriptome and Methylome of Chlamydomonas reinhardtii throughout Its Life Cycle. Plant Physiol 169:2730-43
Geng, Sa; De Hoff, Peter; Umen, James G (2014) Evolution of sexes from an ancestral mating-type specification pathway. PLoS Biol 12:e1001904
Umen, James G (2014) Green algae and the origins of multicellularity in the plant kingdom. Cold Spring Harb Perspect Biol 6:a016170
Fang, Su-Chiung; Chung, Chin-Lin; Chen, Chun-Han et al. (2014) Defects in a new class of sulfate/anion transporter link sulfur acclimation responses to intracellular glutathione levels and cell cycle control. Plant Physiol 166:1852-68

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