Ovarian self-incompatibility inNarcissus papyraceus(Amaryllidaceae) is the result of a pre-zygotic response

Abstract

Ovarian self-incompatibility, including pre-and post-zygotic reactions, is a complex mechanism for which we still lack many details relating to its function and significance. The joint presence of ovarian self-incompatibility with style polymorphism is a rare combination that is found in the genus Narcissus. Usually, style polymorphic species have heteromorphic (diallelic and linked to style length locus) incompatibility, which prevents fertilization between individuals of the same morph, thereby helping to maintain equal proportions of floral morphs in populations. However, when present, self-incompatibility in Narcissus is not linked to style polymorphism and cross-fertilization within each morph is possible. Hence, self-incompatibility in Narcissus is of particular interest when attempting to unravel the nature of the rejection reaction and aiming to assess possible cryptic differences in the fertilization process in intra-and inter-morph crosses, which might ultimately explain the wide variation of morph-ratio in the field. We examined the breeding system of Narcissus papyraceus, a style-dimorphic species that has biased morph ratios in most of its populations. We studied pollen-tube growth in the pistil and ovule fate after experimentally controlled hand pollinations. The growth of pollen tubes in self-and intra-and inter-morph crosses was similar up to the point of micropyle penetration in both morphs but, subsequently, a pre-zygotic failure appeared to affect male and female gametophytes in selfed pistils. A high proportion of ovules from self-pollinated flowers showed signs of collapse and self-pollen tubes were blocked or behaved abnormally before entering the embryo sac. Selfincompatibility was stronger in the long-styled morph than in the short-styled morph. We did not find any conclusive sign of differential functioning between intra-and inter-morph cross-pollinations in any morph. These results enable us to rule out the possible effects of pollen-pistil interactions in N. papyraceus as a cause of morph-ratio biases and confirm the exceptional nature of the self-incompatibility mechanism in this polymorphic species.

Disassortative mating prevails in style-dimorphicNarcissus papyraceusdespite low reciprocity and compatibility of morphs

“…Two factors acting in concert may account for the higher probability of selfing in the S‐morph: the late‐acting self‐incompatibility system of imperfect action of N. papyraceus , which is particularly weak in the S‐morph, and the reduced dichogamy of the S‐morph (Simón‐Porcar et al. ), as previously reported for N. assoanus (Cesaro et al. ).…”

“…The species has a late‐acting self‐incompatibility system of imperfect action (Simón‐Porcar et al. ) similar to that reported in other species in the genus (Dulberger ; Sage et al. ) that permits either between‐ and within‐morph fertilization (Arroyo et al.…”

Associations between sex‐organ deployment and morph bias in related heterostylous taxa with different stylar polymorphisms

“…In species with late-acting ovarian self-incompatibility, self-pollen tubes may disable ovules otherwise available for cross-fertilization, i.e., ovule discounting ( Waser and Price, 1991 ;Barrett et al, 1996 ;Sage et al, 1999Sage et al, , 2006Navarro et al, 2012 ). Whether L. fruticosa possesses a late-acting self-incompatibility system is currently unknown; however, it may be signifi cant that this form of incompatibility has been previously reported in species with stigma-height dimorphism, including members of the Boraginaceae ( Dulberger, 1964( Dulberger, , 1970Philipp and Schou, 1981 ;Schou and Philipp, 1984 ;Barrett et al, 1997 ;Simón-Porcar et al, 2015b ). Th us, reduced herkogamy in the S-morph could conceivably result in lower fi tness of this morph in populations driving its frequency downward.…”

“…In several species of Anchusa , Lithodora, Glandora (Boraginaceae), and Narcissus (Amaryllidaceae) the style morphs are self-incompatible but intramorph compatible-a pattern inconsistent with heteromorphic incompatibility and indicative that they possess distinct self-recognition systems ( Anchusa -Dulberger, 1970 ;Philipp and Schou, 1981 ;Schou and Philipp, 1984 ;Lithodora andGlandora -Ferrero et al, 2011a , 2012 ;Narcissus -Dulberger, 1964 ;Barrett et al, 1997 ;Arroyo et al, 2002 ;Baker et al, 2000b ;Simón-Porcar et al, 2015b ). In Anchusa ( Schou and Philipp, 1983 ) and Narcissus ( Dulberger, 1964 ;Sage et al, 1999 ;Santos-Gally et al, 2015 ;Simón-Porcar et al, 2015b ) self-rejection involves late-acting ovarian incompatibility. Signifi cantly, sex-organ reciprocity is less well developed in these taxa despite clear polymorphism for style length.…”

Breeding systems in Cyrtanthus (Amaryllidaceae): variation in self‐sterility and potential for ovule discounting

“…Inbreeding depression may even reinforce LSI in some plants (Hao et al ). In other cases self‐pollen tubes enter the ovary without fertilisation taking place (Simon‐Porcar et al ), thus ruling out inbreeding depression as an explanation for self‐sterility. LSI has been reported in many woody plants, but this group is also expected to carry high levels of genetic load on account of the relatively high number of mitotic divisions from the zygote to gamete stages (Klekowski ; Scofield & Schultz ), and some cases of self‐sterility in woody plants may therefore be due to very strong early inbreeding depression.…”