The haploid unicellular green soil alga Chlamydomonas reinhardtii has 2 mating types, plus and minus (1). The MT+ and MT- loci, ~400 kb rearranged regions in LG VI, carry genes unique to each mating type. Mitotic cells starved for nitrogen rapidly differentiate into gametes. Expression of the MT- -linked MID gene triggers minus gametes to produce minus agglutinins, minus fusion apparati, and the homeoprotein Gsm1; plus gametes produce plus agglutinins, plus fusion apparati and the homeoprotein Gsp1. Within 10 min of zygote formation, Gsm1/Gsp1 heterodimers migrate to the nuclei and switch on diploid-specific genes, mimicking the haploid-diploid transition pattern in yeast and suggesting that homeoprotein heterodimerization is an ancient sexual strategy (2). The resultant zygotes later undergo meiosis to produce plus and minus progeny. A curious and still unexplained feature of most sexual agendas is their governance of organelle-DNA transmission patterns: progeny receive mitochondrial (mt) and/or chloroplast (cp) genomes from only one parent. In some cases, the zygote initially harbors organelles from both parents and the DNA contributed by one parent is then selectively destroyed while the DNA contributed by the other parent is selectively protected. Destruction/protection systems operate in Physarum (amoeba), Oryzias (fish), mouse, Chlamydomonas (plant), and possibly Cryptococcus (fungus), suggesting that this solution to the “organelle problem” has arisen repeatedly during evolutionary history. In Chlamydomonas, cp genomes from the plus parent are protected while cp genomes from the minus parent are destroyed within 1.5 hr after zygote formation; intriguingly, later in zygote development, mt genomes from the minus parent are protected while those from the plus parent are destroyed. Our studies of the cp system implicate the participation of 4 proteins, all carrying putative or documented cp transit sequences. Protection is apparently conferred by the Otu2 protein, encoded by a reiterated gene family unique to the MT+ locus and expressed only during plus gametogenesis. Misexpression of OTU2 in minus gametes results in protection of minus cpDNA such that meiotic progeny inherit cp markers from both parents (biparental (BP) inheritance). TatD1, a gamete-specific cation-dependent exo/endonuclease expressed in gametes, is a candidate destroyer. Two additional proteins, Ezy1 and Ezy2, expressed within 10 min of zygote formation, appear to be involved in targeting and/or activating the nuclease since inhibiting their expression results in BP inheritance of cp markers. Reiterated copies of EZY1 are found in both the MT+ and MT- loci, whereas EZY2 genes alternate with OTU2 genes in a cluster restricted to MT+. (1) Goodenough, U., H. Lin, and J-H Lee. 2007. Sem. Cell Devel. Biol. 18: 350-361. (2) Lee, J-H, H. Lin, S. Joo, and U. Goodenough. 2008. Cell 133:829-840.