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Darwin's Foundation for Investigating Self-Incompatibility and The Journal of Experimental Botany, Vol. 60, No. 4, pp. 1069–1081, 2009 doi:10.1093/jxb/erp024 DARWIN REVIEW Darwin’s foundation for investigating self-incompatibility and the progress toward a physiological model for S-RNase-based SI Bruce McClure* Division of Biochemistry, Interdisciplinary Plant Group, Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO Downloaded from https://academic.oup.com/jxb/article/60/4/1069/568810 by guest on 01 October 2021 65211-7310, USA Received 31 October 2008; Revised 20 January 2009; Accepted 22 January 2009 Abstract Charles Darwin made extensive observations of the pollination biology of a wide variety of plants. He carefully documented the consequences of self-pollination and described species that were self-sterile but that could easily be crossed with other plants of the same species. He believed that compatibility was controlled by the ‘mutual action’ of pollen and pistil contents. A genetic model for self-sterility was developed in the early 1900s based on studies of the compatibility relationships among, what are now referred to as, self-incompatible (SI) Nicotiana species. Today, it is believed that SI in these species is controlled by an interaction between S-RNases produced in the pistil and F-box proteins expressed in pollen and, moreover, that this S-RNase-based SI system is shared by a great diversity of other plant species. Current research is aimed at understanding how the mutual actions of these S-gene products function in the physiological context of pollen tube growth. Key words: Darwin, self-incompatibility, SFB, SLF, S-RNase. The 200th anniversary of Darwin’s birth and the 150th hypotheses and extend his studies. Darwin’s insight not- anniversary of the publication of Origin of species is a good withstanding, the modern understanding of inheritance—in time to reflect on Darwin’s broad contributions. Darwin’s terms of the unit of transmission, the gene, its chemical family was definitely on the winning side of the industrial nature, the processes of gene expression, and the genomic revolution; he was a grandson of Josiah Wedgwood who and population-level contexts of genes—represents dramatic developed the famous line of manufactured pottery. Given advances that would surely have thrilled him. Thus, this the importance of Darwin’s ideas to modern biology, it is review will also highlight current SI research; insights that a little frightening to consider how contingent they were on this author would share with him, if that were possible. The the whims of history. Nevertheless, it is fortunate that an reader is referred to de Nettancourt’s (1977, 2001) classic intellect of Darwin’s quality ended up in the circumstances monographs and the recent volume edited by Franklin- to travel the world observing and collecting, and then to Tong (2008a) for more in-depth treatments. spend a lifetime in further reflection and experimentation. This review will recall Darwin’s work on self- and cross- pollination, in particular, on what is now called self- incompatibility (SI). The focus will be on progress toward Darwin on heterostyly and self-sterility understanding S-RNase-based SI. Darwin’s own words will Darwin had a very keen interest—expressed on several be used to convey his thoughts and his fascination with levels—in plant reproduction. He published two editions on many of the same questions that ignite students today. The pollination of orchids (Darwin 1862, 1877a), but the works insights are often uncanny, and researchers interested in most relevant here are The different forms of flowers on population-level studies still find it productive to test his plants of the same species, published in 1877, and The effects * To whom correspondence should be addressed. E-mail: [email protected] ª The Author [2009]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: [email protected] 1070 | McClure of cross and self-fertilisation in the vegetable kingdom, first published in 1876 with a second edition in 1878. He was well aware of earlier works (especially by Ko¨lreuter, Mu¨ller, and Scott) that described instances of what we now refer to as SI. An early paper on self-sterility by EM East includes a useful review of this early work (East and Park, 1917). Darwin’s later work shows that he was definitely excited by the variety and the subtlety of plant reproduction. There is hardly anything more wonderful in nature than the sensitiveness of the sexual elements to external influences, and the delicacy of their affinities..We see how sensitive the sexual elements of those plants must be, which are com- pletely sterile with their own pollen, but are fertile with that of any other individual of the same species. (Darwin, 1878; Downloaded from https://academic.oup.com/jxb/article/60/4/1069/568810 by guest on 01 October 2021 p. 467) In The different forms of flowers, Darwin discusses many instances where a single species elaborates alternative floral Fig. 1. Legitimate and illegitimate pollination in Primula. The figure morphologies, but plants that display, what is now referred is reproduced from Darwin (1877b). Reproduced with permission to as, heteromorphic SI capture the most attention. Hetero- from John van Wyhe, ed., The complete work of Charles Darwin styly in Primula and its relatives is the best known system. online (http://darwin-online.org.uk/). His passion for comprehensive, meticulous observation and experimentation is clearly expressed. Darwin describes the differences between floral morphs in great detail, including On a more theoretical level, Darwin recognized the pollen size and appearance, organ positioning and size, and importance of restricted mating and described it as a mech- stigma papillae. He experimentally probes the function anism for dividing a population into distinct ‘bodies’ of of organ positioning, but he finds, importantly, that it is compatible partners. not sufficient to ensure that crossing occurs only between (W)e have here a case to which no parallel exists in the morphs: vegetable or, indeed, in the animal kingdom. The individual plants of the present species, and as we shall see of several It follows from the position of the organs that if the proboscis other species of Primula, are divided into two sets or bodies, of a dead humble-bee, or a thick bristle or rough needle, be which cannot be called distinct sexes, for both are hermaph- pushed down the corolla, first of one form and then of the rodites; yet they are to a certain extent sexually distinct, for other, as an insect would do in visiting the two forms growing they require reciprocal union for perfect fertility. (Darwin, mingled together, pollen from the long-stamened form 1877b; p. 28) adheres round the base of the object, and is left with certainty on the stigma of the long-styled form; whilst pollen from the He also understood that mating was subject to natural short stamens of the long-styled form adheres a little way selection and that heterostyly had emerged independently in above the extremity of the object, and some is generally left on different plant lineages at different times. Furthermore, he the stigma of the other form. In accordance with this conducted experiments showing the benefit of outcrossing observation I found that the two kinds of pollen, which could and the ‘evil’ of selfing in many species. He perceived that easily be recognised under the microscope, adhered in this the benefit of outcrossing within a species was sufficient to manner to the proboscides of the two species of humble-bees select for emergence of incompatibility systems. Barret and and of the moth, which were caught visiting the flowers; but Shore (2008) emphasize that a more developed view takes some small grains were mingled with the larger grains round account of different benefits of heterostyly per se versus the base of the proboscis, and conversely some large grains intramorph incompatibility; the former reduces pollen waste with the small grains near the extremity of the proboscis. Thus pollen will be regularly carried from the one form to the by facilitating its placement on receptive stigmas while other, and they will reciprocally fertilise one another. The incompatibility prevents inbreeding and contributes more several foregoing facts led me to try the effects of the two to maternal fitness. kinds of pollen on the stigmas of the two forms. (Darwin, We may feel sure that plants have been rendered hetero- 1877b;p.24) styled to ensure cross-fertilisation, for we now know that His experiments revealed that intermorph (i.e. legitimate) a cross between the distinct individuals of the same species is pollinations were fully fertile while intramorph (i.e. illegiti- highly important for the vigour and fertility of the offspring. (Darwin, 1877b; p. 258) mate) pollinations set few seed. Figure 1, reproduced from Darwin’s book, shows these relationships diagrammatically; (W)e may confidently believe that this has been effected in this figure has been so frequently imitated by subsequent order that cross-fertilisation should be assured. For the full generations of scholars that any student of pollination will and legitimate fertilisation of these plants pollen from the recognize it. one form must be applied to the stigma of another.. There Progress toward a model for S-RNase-based SI | 1071 is reason to believe that the sterility of these unions has not same result been confirmed by several subsequent trials. been specially acquired, but follows as an incidental result (Darwin, 1878; p. 188) from the sexual elements of the two or three forms having been adapted to act on one another in a particular manner, It is clear that Darwin found self-sterility noteworthy and so that any other kind of union is inefficient, like that appreciated its potential significance.
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