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A Genetic Map Ofnon-Mendelian Genes in Chlamydlomonas* Ruth Sager and Zenta Ramanis

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A Genetic Map Ofnon-Mendelian Genes in Chlamydlomonas* Ruth Sager and Zenta Ramanis Proceedings of the National Academy of S&ienes Vol. 65, No. 3, pp. 593-600, March 1970 A Genetic Map ofNon-Mendelian Genes in Chlamydlomonas* Ruth Sager and Zenta Ramanis DEPARTMENT OF BIOLOGICAL SCIENCES, HUNTER COLLEGE OF THE CITY UNIVERSITY OF NEW YORK Communicated by E. L. Tatum, December 22, 1969 Abstract. A group of eight non-Mendelian genes have been shown by re- combination analysis to be linked into a linear structure or chromosome. Similar genetic maps of gene order and relative distances between genes have been con- structed by two methods, one based on additivity of recombination frequencies, the other on frequency of reciprocal recombination with a postulated attachment point. The data indicate that the progeny are diploid for this linkage group, and that the strands are distributed in a precisely oriented manner at mitosis. Evidence is discussed in support of the view that this linkage group is located in chloroplast DNA. In this paper we present evidence that a set of non-Mendelian genes in Chlamy- domonas can be mapped into a linear linkage group. The first non-Mendelian gene was described in 1908 by Carl Correns.1 Numerous examples of non-Men- delian heredity have been reported in the intervening sixty years,2 but this paper provides the first evidence that non-Mendelian genes are organized into chromo- some-like structures that can be mapped by formal genetic methods. The first instance of recombination between two pairs of non-Mendelian genes was reported in 1963,3 the same year in which the presence of DNA in chloroplasts and mitochondria was established.4 Although knowledge of the presence of organelle DNA did not contribute directly to the genetic analysis reported here, correlations between the behavior of these genes and their DNA's will be of central importance in further studies. It is likely, as discussed below, that the linkage group described here is physically located in chloroplast DNA. The long lag in developing non-Mendelian genetics resulted in part from two obstacles: (1) the difficulty in obtaining non-Mendelian mutations, and (2) the maternal pattern in inheritance typical of non-Mendelian genes, which precludes recombination analysis and mapping. Methods for overcoming these obstacles were developed with Chlamydomonas.3 5 We found that cells suitably treated with streptomycin give rise to mutations of non-Mendelian genes but to virtually no mutations of nuclear genes.5 Despite its spectacular effectiveness, the molecular basis of this differential mutagenic action of streptomycin is not known. Maternal inheritance has been the key to the identification of non-Mendelian genes but has also been a serious impediment to their further study. In Chlamy- domonas we discovered that UV irradiation of the female parent immediately before mating would effectively block maternal inheritance under conditions of 593 Downloaded by guest on September 29, 2021 594 GENETICS: SAGER AND RAMANIS PROC. N. A. S. little or no lethality.7 With UV irradiation we can routinely produce biparental progeny with non-Mendelian genomes from both parents. These progeny provide the material for recombination analysis. Materials and Methods. Mutants: The non-Mendelian genes ac1 and ac2 repre- senting respectively leaky and stringent requirements for acetate were described before, as were sm2 (previously called sr, resistant to 500 ,g streptomycin per ml) and sm4 (previously called sd, streptomycin-dependent). Sm3 is a low-level streptomycin- resistant, nea is a neamine-resistant, obtained from N. R. Gillham who calls it nr, and ery is resistant to 50 og erythromycin per ml. Csd is a conditional mutant, requiring streptomycin to grow at 350C. Crosses: The studies to be reported here were carried out with the following crosses: Cross 1: 6978a (aC2+ acW sm3-s Sm2-scsd-s) X 7018g (ac,ac2 + sm3-r sm2-r csd-r) Cross 2: 11108-5 (ac2+ ery-r sm2-s) X 7018g (ac2 ery-s sm2-r) Cross 3: 229-3-4 (ac2+ ac( sm4-d ery-e sm2-s) X 11209-5 (ac2 aC + SM4-s ery-r sr2-r) Cross 4: 229-3-4 (ac1 sm4-d nea-s 8m2-8) X 12-6-2 (acl+ =f4-8 nea-r sm2-r) Cross 5: Z-12-4 (aC2+ ery-s nea-r smrs) X 11154-4 (aC2 ery-r nea-s sm2rr) Other crosses are listed in Table 3. Each parental pair also differs in three pairs of un- linked chromosomal genes (actidione resistance, methionine sulfoximine resistance, and mating type); these genes segregate in meiosis as previously described and provide a means for identifying the four zoospore products of meiosis. Crossing procedure: Gametes were prepared as previously described.6 Plus mating type (female) gametes received 40 sec of UV irradiation, and were then mated in the dark with unirradiated males. After 2 hr, the suspensions of newly formed zygotes were plated at suitable dilution, kept in light for 24 hr, and then incubated in the dark for 5 to 10 days. Synchronous germination was induced by exposure to light. After one mitotic doubling, clusters of 8 0 x octospores derived from single zygotes 0 were transferred to fresh plates where a PI l + P2 second doubling occurred. The cells were then respread so that the colonies derived from pairs of octospore daughter Zygote cells could be identified. By this pro- + cedure we obtained pedigrees of the first G3 o o two doublings of each zoospore, as 2 3 4 shown in Figure 1. Progeny cells were TetrasporesTetrospores grown to form colonies which were then 6' 6' 6' \b 6' \b classified for all markers.6' 7 la blb 2a \b2b 3a 3b 4a 4b Studies of closely linked genes: Octospores ' ' Results of cross 1 are shown in Tables 1 and 2. Zoospores were lol 1a2 fbl 0b2 2al 202 2bl 2b2 3al 3a2 3bl 3b2 4al 4a2 4b1 402 heterozygous for all four segregat- Octospore Daughters ing markers, as described in pre- FIG. 1.-Procedure for pedigree analysis. Ga- vious studies,6 8 and the appearance metes are mated and zygotes plated as noted in of pure homozygotes began at the the text. After germination, progeny of indi- first mitotic doubling. As shown in vidual zygotes are replated at the octospore stage and after one more doubling each pair of octo- Table 1, after two doublings 60-70 spore daughter cells is separated and allowed to per cent of the progeny were still form colonies. The 16 colonies, representing the heterozygous for one or both genetic first two doublings of each zoospore, are then classified for all segregating markers. regions. In a previous study of Downloaded by guest on September 29, 2021 VOL. 65, 1970 GENETICS: SAGER AND RAMANIS 595 TABLE 1. Segregation and recombination of closely linked genes (Cross 1). ac2+ aC sMr-s sm2-s X ac2 acl+ 8mrr smg-r A-Acetate Region Remaining Parental Segregants Recombinants hets* (%) (%) (%) ac2+ acl ac2 aci + ac2 + aci + ac2 + aci Total acg+ aci acgaci + aC2 + acg aci r Expt. 1 1419 13.2 10.4 2.1 74.4 Expt. 2 559 16.5 17.5 2.2 64.0 B-Streptomycin Region Remaining Parental Segregants Recombinants hets* (%) (%) (%) 8mg-s 8m2-8 8mg-r 8m2-r smg-fr 8mg2-s 8mg-8 8m-s Total 8mg-s 8m2-8 8msg- 8m2-r 8mg-r Sm2-8 8mg-r 8mg-r Expt. 1 1419 14.2 10.6 4.4 71.0 Expt. 2 559 21.2 18.6 2.5 57.8 Scored as per cent of total progeny after two mitotic doublings of zoospores. * May include additional genotypes which are phenotypically het, such as acg + ac +/ac2 acg and SM3- 8mg-rin/&M-f M2-8. TABLE 2. Linkage of acetate and streptomycin regions (Cross 1). Progeny class Recombination Numbers of Progeny$ 1 2 3 region Expt. 1 Expt. 2 Expt. 3 ac2+ ac1 Smg-s 8mg-s Parental 75 32 66 ac2 ac1 + smg-r sm2-r Parental 64 36 52 aC2+ ac1 smg-r smg-r 2 13 7 71 ac2 ace+ 8mgs siM2-s 2 20 15 57 acg+ ac1 smg-r smgs 2 + 3* 13 0 nst aeg ac1 + Smg-r s8M-s 3 15 6 ns ac2+ aci+ sn-r sm2-r 1 7 2 7 ac2+ aci+ 8mrs 8mg-s 1 + 2 5 3 8 ac2+ ac+smvr8smg-s 1 + 3 2 0 ns Total progeny segregated 214 101 261 Recombination in Region 1 6.5 5.0 5.8 2 23.9 25.0 52.2 3 14.0 6.0 ns * Position of 8mg- between acg and sn2 assigned on basis of data in Table 3 and unpublished. t ns = not scored. t Expt. 1 and 2 same as Table 1; Expt. 3 scored after 4 to 6 doublings. this cross8 we showed that the rate of segregation in these genetic regions is constant, with the surviving fraction of heterozygotes decreasing exponentially. No genetic class of persistent heterozygotes has been detected. In Table 1, the ratio of parental alleles among the progeny after two doublings appears to be close to 1:1 in both regions. The new classes ac+ ac2+ and sm3-r sm2-s are recombinants. The reciprocal recombinants are present but special methods are required to detect them, and they cannot be readily enumerated. The ac1-ac2 double mutant is phenotypically like ac2 and has been identified genetically.6 The sm3-s sm2-r recombinant is phenotypically like the double resistant; it has also been identified genetically.9 Linkage between acetate and streptomycin regions: The classes of progeny obtained in cross 1 have been listed in Table 2, together with the numbers of Downloaded by guest on September 29, 2021 596 GENETICS: SAGER AND RAMANIS PROC.
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