This Week’s Citation Classic* Lewis D. Comparative incompatibility in angiosperms and fungi. Advan. Genet. 6:235-85, 1954. [John Innes Horticultural Institution, Bayfordbury, Hertford, Hertfordshire, England] CC/NUMBER 35 SEPTEMBER 1, 1986 A comparative and comprehensive treatment is given for seven genetic systems of self-incompatibility, four in flowering plants and three in fungi. [The SC/®_in- dicates that this paper has been cited in over 160 publications since 1955.) D. Lewis School of Biological Sciences Queen Mary College University of London London E1 4NS England July 8, 1986 ~ This review summarized 18 years of my work and thought at the John innes Horticultural Institution. Self-incompatibility was, and still is, important in fruit production and was of genetical interest because the controlling gene had many alleles, each conferring a unique recognition between pollen and style. 1 was given complete freedom to work and started to show that the striking effect of autotetraploidy that nullified the recognition process and made a plant self-compatible was due to interactions be- tween the products of different alleles in diploid polien. By serological methods, the !-gene product was shown to be a serologically active protein. Us- ing the self-style as a highly sensitive selector of I- gene mutations, | showed that the gene was a com- plex of two and probably three closely linked genes, one active in the pollen and another in the style; all the mutations were to loss of activity to self-com- patibility. No new active alleles were found despite the sensitivity of the method to 10° and the large number of alleles in wild populations. This caused some controversy about the efficiency of the style for selecting new active alleles, which might be the result of a series of mutational changes in the genome. All this and much work of others was set in con- text in the review. But.an important factor in the timeliness of the review was the discovery of the new sporophytic system by Babcock and Hughes! and Gerstel? in the US, and Bateman? and Crowe! in my own laboratory. This system combined multiple alleles with maternal control of the poilen, a hypothetical combination that | had foreseen’ but arrogantly dismissed as improbable and beyond the capacity of the gene, a mistake | hope not to make again. oi were included in the review because of the frustration of not-finding active new allelic mutants in plants. 1 turned to the higher fungi, which have a similar multi-allelic system and a more direct cellular barrier. A Coprinus species. collected from the wild was.the foundation stock of what became a standard genetic organism in several laboratories. But, even in this organism, only breakdown mutants rather than allelic mutants were obtained. The review also described the application of self-incompatibility to plant improvement. The com- mercial production of F, hybrid vegetables was the outcome of the new sporophytic system. The com- mercial exploitation of my own self-compatible mutants of the sweet cherry, Prunus avium, has left me with only the review and mixed feelings. The practical application in Britain suffered from politi- cal considerations and what the late C.D. Darlington called the “dead hand on discovery.’ Fortunate- ly, the unique Ic gene was sent to the Canadian Department of Agriculture and developed by Lapins into the first commercial self-compatible sweet cherry, Stelfa.® My work was recognised one year after the review by my election to Fellowship of the Royal Society and later by my invitation to the Quain Chair of Botany at University College London. The originality and significance of the review were mainly in its comparative approach, which was en- hanced by the treatment of four different genetic sys- tems, including the newly discovered sporophytic system, in plants and three systems in fungi. it may be significant that de Nettancourt, in his specialist book on the subject,? makes 141 refer- ences in the text to 24 of my papers. The “classical” review is referred to only five times. The most fre- quently quoted is a paper with a highly contentious hypothesis on unilateral incompatibility that stimu- lated many disparagements.'9 It would appear from this that the main reason for the high rating of a re- view is that it is (too often) an easy way of quoting the literature with the added bonus of an authorita- tive backing for quotation. L have, with S.C. Verma and M.I. Zuberi (manu- script), recently reexamined the sporophytic system and have found a second gene G that is complemen- tary to the well-established S gene and is gametophyt- ic in its action, Current work of others has turned to molecular aspects and gene isolation; the most re- cent contribution"! is a good example and contains useful references to recent research and reviews. A J. Seif-incomp in Crowe L K. Incompatibility in Cosmos bipinnamus. Heredi Besuanevunr (Cited 120 times.) . Hughes M B & Babcock E B. Self-incompatibility in Crepis foetida L. subsp. rhoedaifolia. Generics 35:570-88, 1950. . Gerstel D V. Self- incompatibility studies in Guayule. I. Inheritance. Genetics 35:482-506, 1950. - perms. HI. Iberis amara. Heredity 8:305-32, 1954. 8:1-11, 1954. Lewis D. Incompatibility in plants: its genetical and physiological synthesis. Nature 153:575-8, 1944. Darlington C D. The dead hand on discovery. I. The fingers of learning. Discovery 9:358-62, 1948. ————.. The dead hand on discovery. Il. The thumb of office. Discovery 10:7-11, 1949. Brown A G. Cherry Stella’ Garden J. Roy. Hort. Soc. 108:277, 1983. . de Nettancourt D. /ncompatibiliry in angiosperms. Berlin: Springer-Verlag, 1977. 230 p. . Lewis D & Crowe L K, Unilateral interspecific incompatibility in flowering plants. Heredity 12:233-56, 1958. . Anderson M A, Cornish E C, Mau S-L, Williams E G, Hoggart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche P L Haley } D, Penschow J D, Niall H D, Tregear G Ww, Goghlan J P, Crawford R J "& Clarke A'E. Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata. Nature 321:38-44, 1986. CURRENT CONTENTS® ©1986 by |SI@ 43 eee