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Francisco J. Valtue Ñ a 2 , Tom Á S Rodr Í Guez-Ria Ñ O 2 , Francisco

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Francisco J. Valtue Ñ a 2 , Tom Á S Rodr Í Guez-Ria Ñ O 2 , Francisco American Journal of Botany 97(1): 123–135. 2010. S ELF-STERILITY IN TWO CYTISUS SPECIES (LEGUMINOSAE, PAPILIONOIDEAE) DUE TO EARLY-ACTING INBREEDING DEPRESSION 1 Francisco J. Valtue ñ a 2 , Tom á s Rodr í guez-Ria ñ o 2 , Francisco Espinosa 3 , and Ana Ortega-Olivencia 2,4 2 Á rea de Bot á nica, Facultad de Ciencias, Universidad de Extremadura, Avda. de Elvas, s.n. 06071-Badajoz, Spain; and 3 Á rea de Fisiolog í a Vegetal, Facultad de Ciencias, Universidad de Extremadura, Avda. de Elvas, s.n. 06071-Badajoz, Spain In most angiosperms, the endosperm develops before the embryo, but with harmony between the two structures until fi nal seed formation. In an embryological study, we show that inbreeding depression causes disharmony in development of the two structures in two Leguminosae shrubs, Cytisus multifl orus and C. striatus. Our main objective was to test the causes of self-sterility in the two species by comparing the embryological development of the self seeds with that of cross seeds. In developing selfed seeds of C. multifl orus , the embryo reaches at most the globular stage and never forms mature seeds, while in C. striatus a few mature selfed seeds are formed. In both species, the main cause of abortion of developing selfed seeds is diminished endosperm develop- ment (low values of the ratio of endosperm to embryo), which triggers collapse of the endosperm and embryo. The results indicate that self-sterility in C. striatus is postzygotic because of strong, early inbreeding depression, while in C. multifl orus there exists a mixed pre- and postzygotic mechanism; the prezygotic mechanism causes rejection of some self-pollen tubes in the style/ovary, and the early inbreeding depression triggers abortion of fertilized ovules that escaped that action. Key words: abortion; Cytisus multifl orus ; Cytisus striatus ; embryogeny failures; inbreeding depression; late-acting self-in- compatibility; Leguminosae; Mediterranean region; self-sterility. The two principal mechanisms that induce self-sterility in lemoniaceae, Convolvulaceae, Caryophyllaceae, and Malva- plants are self-incompatibility (SI) and early-acting inbreeding ceae ( Hiscock and Mclnnis, 2003 ), but at a molecular level the depression (ID). Self-incompatibility involves a series of physi- phenomenon has been very rarely investigated (e.g., Brassica ; ological mechanisms that prevent reproduction after self-polli- see revision in Charlesworth et al., 2005 ). nation or between genetically closely related individuals. This In gametophytic SI, the pollen is controlled by its own geno- mechanism is not only one of the most important means of side- type, and rejection can occur either on the style, more fre- stepping autogamy and of promoting the generation of new quently, or on the stigma. Gametophytic SI is more widespread genotypes among plants, but also it may contribute to angio- than sporophytic SI and is found in families such as Legumino- sperm diversity and success ( de Nettancourt, 2001 ). sae, Scrophulariaceae, Rosaceae, Solanaceae, Papaveraceae, In the SI process, the ovules are not fertilized because of an and Poaceae. At a molecular level, however, the phenomenon active rejection of the male gametophytes that carry the same S has been studied only in Solanaceae, Papaver , Antirrhinum , alleles of the sporophyte ( de Nettancourt, 2001 ). There are basi- and Rosaceae (Silva and Goring, 2001; Franklin-Tong and cally two kinds of prezygotic SI (i.e., prior-to-fertilization): het- Franklin, 2003 ; Charlesworth et al., 2005 ). eromorphic and homomorphic. In heteromorphic or diallelic SI, A third kind of SI, late-acting or ovarian SI ( Seavey and fl owers differ in morphology (i.e., they are heterostylous), Bawa, 1986 ), occurs in two large groups of species. In the fi rst whereas in homomorphic SI, fl owers are not morphologically group of species, pollen tubes reach the ovary after self-pollina- differentiated. tion and can even penetrate the ovules, but fertilization does not Homomorphic SI is much more common ( Richards, 1986 ) take place. This type of rejection is consequently prezygotic. In and can be divided into sporophytic and gametophytic. Sporo- the second group of species, self-fertilization takes place with phytic SI is controlled by the genotype of the pollen-producing subsequent postzygotic rejection ( Seavey and Bawa, 1986 ; plant, and inhibition usually takes place on the stigma surface Gibbs and Bianchi, 1993 ). Because the expression “ late-acting ( de Nettancourt, 2001 ). This type of SI has been recorded in SI ” assumes that rejection is under genetic control similar to families such as Brassicaceae, Asteraceae, Betulaceae, Po- typical mechanisms of prezygotic SI and because these mecha- nisms have not yet been fully determined, some researchers prefer to use other terms, such as ovarian sterility ( Sage et al., 1 Manuscript received 1 October 2008; revision accepted 23 September 1994 ) or pistillate sorting ( Bertin et al., 1989 ). The latter has 2009. been used to describe those cases in which not only the time of The authors thank Dr. M. Gonz á lez (University of Extremadura) for occurrence of syngamy is unknown, but also whether abortion statistical assistance. Suggestions and comments by two anonymous takes place before or after syngamy. The expression involves reviewers and the associate editor greatly improved the manuscript. This no presumption about the control mechanisms of those events work was fi nanced by the Ministry of Education and Science of Spain (maternal, paternal, zygotic, or some combination of these) (projects BOS2002-00703 and CGL2005-00783/BOS, both co-fi nanced by ERDF). A predoctoral grant from that Ministry to F.J.V. (BES-2003- ( Sage et al., 1994 ). Nevertheless, Lipow and Wyatt (2000) 2187) is greatly appreciated. demonstrated in Asclepias exaltata the existence of a single lo- 4 Author for correspondence ([email protected]) cus with polyallelic control of late-acting SI. Inbreeding depression (ID) is defi ned as fi tness loss as a re- doi:10.3732/ajb.0800332 sult of self-fertilization or fertilization between similar or 123 124 American Journal of Botany [Vol. 97 closely related genotypes. This phenomenon is one of the most sis and prepared to receive the pollen tube ( Rodr í guez-Ria ñ o et signifi cant factors infl uencing the evolution of plant reproduc- al., 2006 ); their mature seeds have an aril with a funicular origin tive systems ( Lloyd, 1980 ; Charlesworth and Charlesworth, ( Rodr í guez-Ria ñ o et al., 2006 ). Cytisus multifl orus presents 1987 ). There is a tendency for ID to be particularly intense be- two fl oral morphs, LF (with large fl owers) and SF (with small tween fertilization and the mature seed phase (early ID) when fl owers), with SF having the greater reproductive success of the numerous essential genes are expressed for the fi rst time two ( Rodr í guez-Ria ñ o et al., 2004 ). In this work, we shall only ( Meinke, 1991 ; Seavey and Carter, 1994 ; Husband and Schem- study the more widespread SF. Both species are clearly xenoga- ske, 1996 ). mous and pollinated by bees. Self-sterility in these two species As Seavey and Bawa (1986) observed, it is very diffi cult to is characterized by virtually no seed production and high rates distinguish which effects are attributable to late-acting SI and of abscission of fruits that contain ovule-seeds of varying sizes which to ID. The following two principal criteria have been ( Rodr í guez-Ria ñ o et al., 1999 , 2004 ). Variability in the timing suggested for differentiating between the two biological phe- of fruit abscission and seed abortion indicates that ID may be nomena ( Seavey and Bawa, 1986 ; Sage et al., 1994 ; Nic operating in both species ( Rodr í guez-Ria ñ o et al., 1999 , 2004 ). Lughadha, 1998 ; Lipow and Wyatt, 2000 ): (1) Timing of In addition, prezygotic SI also contributes to self-sterility in C. abortion. A uniform failure at a single developmental stage striatus as indicated by low rates of ovule penetration would be interpreted as late-acting SI, whereas a series of fail- ( Rodr í guez-Ria ñ o et al., 1999 ). However, verifi cation of ID or ures throughout embryogeny would be seen as the result of late-acting SI as the cause of self-sterility remains to be demon- ID. Nonetheless, there have been relatively few studies inves- strated. The main objective of this study is to assess seed devel- tigating embryological processes to confi rm that fertilization opment after cross- and self-pollination to determine whether has occurred before the abortion of the developing seeds (but postzygotic self-sterility in C. multifl orus and C. striatus is due see Gibbs and Bianchi, 1993 ; Seavey and Carter, 1996 ; Gibbs to ID or late-acting SI. Previously published data ( Rodr í guez- and Sassaki, 1998 ; Nic Lughadha, 1998 ; Bittencourt et al., Ria ñ o et al., 1999 , 2004 ) and unpublished data for the years 2003 ; Pound et al., 2003 ; Sage and Sampson, 2003 ). (2) The 2004 and 2005 will be considered in the Discussion. amount of variability in selfed seed set among individuals of a population. Null or almost null seed production after self- MATERIALS AND METHODS pollination in all the individuals of a population would indi- cate late-acting SI, whereas variations among individuals in Plant material— Populations of both Cytisus species ( C. multifl orus and C. the population would be seen as the result of ID. Nevertheless, striatus ) are located at the El Hito estate, in the municipal district of Alburquer- genotypes with a high load of lethal genes could also induce que (Badajoz, SW Spain). The population (39 ° 13 ′ N, 6 ° 57 ′ W) is situated be- complete or almost complete self-sterility ( Seavey and Bawa, tween 390 and 395 m a.s.l. on a granitic substrate and subject to a typical 1986 ; Waser and Price, 1991 ).
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