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    Nasrallah 2017

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    ELSEVIER ‘Available online at www.sciencedirect.com ScienceDirect Genetics aero, Plant mating systems: self-incompatibility and evolutionary transitions to self-fertility in the mustard family June B Nasrallah Flowering plants have evolved diverse mechanisms that promote outcrossing. The most widespread of these outbreeding devices are so-incompatibilty systems, the highly selective prefertiization mating barirs that prevent selt- fertilization by disrupting pollen-pstl interactions. Despite the advantages of outcrossing, loss of settincompatibilty has ‘occurred repeatedly in many plant families In the mustard {amiy, the highly polymorphic receptors and ligands that mediate the recognition and inhibition of se-pollen in self incompatibility have been characterized and the 3D structure of the receptor-igand complex has been solved. Sequence ‘analyses and empirical studies in satincompatile and sel- ‘compatible species are elucidating the genetic basis of ‘itches from the outcrossing to selfing modes of mating and beginning to provide clues to the diversification of the self recognition repertoke. ‘Adress Section of Pant Biology, Schoo of Integrative Plant Science, Come Unversity, Ithaca, NY 14850, Unted States of America Corresponding author: Nasrallah, June 8 (n2@corneliec) ‘Current Opinion in Genetics & Development 2017, 47:54-60 ‘This review comes from a themed issue on Evolutionary genetics. cited by Erie S Haag and David L Stem For a complete overview see the issue and the Ecol ‘Aalabie online 13th September 2017 itp. do.org/10.1016/.9c6.2017.08.005 (0950-437X/= 2017 Esover Lic, Al ights reserved. Introduction In plants as in other organisms, mating system determines. patterns of genetic variation and has profound conse- quences for the rate and mode of evolutionary change. Outerossing is advantageous because it ean produce new ‘combinations of different sequence variants, thus result- ing in the high levels of genetic variability required for adaptation in the face of a wide range of environmental challenges. Yet, the transition from an outcrossing to selfing mating system is one of the most prevalent evolu tionary transitions in flowering plants [1]. This transition ‘occurred repeatedly in many plant families likely because selfing provides transmission advantage aver outcrossers ‘Current Opinion in Genetics & Development 2017, 47:54-60 as well as reproductive assurance when mating partners oF pollinators are searce [2,3]. Consistent with the advantages provided by an outeross- ing mode of mating, flowering plants have evolved an extraordinary variety of adaptations that promote out- crossing, ‘These adaptations include physical separation of the sexes in different individual plants or of male and female lowers on the same plant, ot temporal separation in the maturation of male and female reproductive struc- tures [5]. However, most flowering plants have hermaph- roditie flowers, in which the sperm-carrying pollen grains are in close proximity to the pisil, the female reprod tive structure that harbors the egg cell-containing ovules (Figure 1). Nevertheless, many ofthese plants are obligate or predominant outcrossers, often due to the operation of a genetically determined physiological prefertilization bar rier to self pollination known as self-incompatbility (SD. SI systems, which occur in approximacely half of flowering plane taxa, allow cells ofthe pistil to discriminate between “self and “non-self pollen grains or pollen tubes. The result isa highly specie distuption of pollen germination atthe stigma surface or of pollen tube growth within the pistil (Figure 1), which precludes fertilization and seed produetion in self-pollinations but notin cross-pollinations. Despite these similar outcomes, the underlying mecha- nisms and the genes responsible for pollen recognition and inhibition ean differ in different plant families [4]. Thus, SI refers o a group of independently evolved and mole larly unrelated mechanisms for preventing sel-fertlizaion in hermaphroditie plants. Here, the focus is on the molecular genetic analysis of SSI and mating system transitions in the mustard (Brassi- caceae) family. ‘This family includes self-incompatible obligate outerossers, such as the economically important Brasssica oleracea and B. rapa crop species and wild Arabidopsis Iyrata and A. haleri, as well as predominantly selfing species, such as the ‘model plant Arabidopsis thaliana. The review summarizes our curtent understand- ing of the molecular basis of self-pollen recognition and of the genetic basis of switches from SI to self-fertlity in the family, and presents daca related to the diversification of the SI recognition repertoi Sl in the mustard family The features of SI in the mustard family have been extensively reviewed [5]. In brief, a distinctive feature of SI in this family is chat self-pollination is inhibited at ‘wow eloncedoet.com Figure Evolution of plant mating systems Nasrallah 55 © @ Polinaton responses inthe mustara family. a) An Arabidopsis thalana flower showing th family, The arrow points fo the stgms, wich i he sbucture the pst and te path af pole tube grou The panel on the left shows a Scanning Election Meroscopy (SEM) mage inch consists ofa stigma, syle, and ovary. The panel on the right shows a UV fuorescence mcroscope image ofa polinated ps fur potas that are characteristic of the overshelming a interacts with incoming poten grains, (a) Structure of the A thalana pt ‘lorescent tubes growing trough pst tesues, For successful fertization to occur, apolen gain, which ie released ina dessicated site from the anthers, must hyerate a the sigma surface and germinate te produce a pole tube that grows into the wal ofa stigma epidermal cell ane wut the extracellar matrx a ho sile and evar. Inthe avay, the poll tube ls guided totard an ovuointo which releases ie sperm coll, resulting in fertilzaion ang seed production. e) An SEM image showing he nteracton of a germinated pollen gran (Po) wit a stigma epidermal ‘el (SE), mage courtesy of MK Kandasamy.(f) The otoomee of crose-plinaton and zet-polinaton ina sefncomptible plat. Note that pen cross-poinaton {ei large numbers of elongated pollen tubes are produced, By corirat, upon sel-poiration (igh, pollen gains are ‘rested atthe stigma surface and any pllen tubes that do frm fal to elongate and grow into the pi the surface of stigma epidermal cells within minutes of pollen-stigma contact, primarily due to the failure of self pollen grains to hydrate and germinate (Figure 1). Con- sistent with this rapid and specific inhibition of self pollen, two self-recognition genes have been identified at the locus, designated ‘S', which determines pollen recognition specificity: one gene encodes the S-locus receptor kinase (SRK), a single-pass transmembrane ser ine/thrconine kinase displayed on the plasma membrane ‘of stigma epidermal cells; and the second gene encodes the S-locus cysteine-rich protein SCR (also designated SP11),a small (~50 amino acids) diffusible component of the pollen coat that is the ligand for SRK. Together, SRK and SCR comprise the SI specificity-determining 5 hap- lotype and are the sole determinants of specificity in the SI response. The SRK and SCR proteins exhibic extra dinarily high levels of polymorphism and their genes show clear signs of co-evolution [6]. ‘The interaction between SRK and SCR is haplotype-specific and ic is this interaction chat determines specificity in the SI response and criggers a cascade of events within che stigma epidermal cell chat culminates in the inhibition of selfpollen (Figure 1 [7)). ‘Thus, the persistence of ST depends on the maintenance of co-adapted SRK and SCR alleles ina tightly linked genetic unit. This linkage appears to be maintained by small physical distances between the two genes in some cases [8], or more frequently, by suppressed recombination in the S-locus region. Indeed, 5 haplotypes typically differ in overall size and organization, they contain haplorype-specific sequences, and they accumulate transposable element sequences, similar

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