A Dual Role for the <i>S</i>-Locus Receptor Kinase in Self-Incompatibility and Pistil Development Revealed by an <i>Arabidopsis rdr6</i> Mutation

Tantikanjana, Titima; Rizvi, Noreen F.; Nasrallah, Mikhail E.; Nasrallah, June B.

doi:10.1105/tpc.109.067801

Cited by 49 publications

(58 citation statements)

References 53 publications

(72 reference statements)

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“…In this study, the approach herkogamous phenotype in wild-type A thaliana was only observed when ARC1 was expressed with the SCRb-SRKb construct, suggesting that SRKb with ARC1 is required for this trait. Interestingly, SRKb was previously found to cause a stigma exertion phenotype when expressed in the Arabidopsis mutant for the RNA-dependent RNA polymerase-6 (rdr6) (Tantikanjana et al, 2009). However, we do not know if the approach herkogamy phenotype that we observed in wild-type A. thaliana expressing ARC1 with SCRb-SRKb results from a related mechanism to that seen for the stigma exertion phenotype Numbers indicate the number of samples.…”

Section: Discussionmentioning

confidence: 99%

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The ARC1 E3 Ligase Promotes Two Different Self-Pollen Avoidance Traits inArabidopsis

2014

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Flowering plants have evolved various strategies for avoiding self-pollen to drive genetic diversity. These strategies include spatially separated sexual organs (herkogamy), timing differences between male pollen release and female pistil receptivity (dichogamy), and self-pollen rejection. Within the Brassicaceae, these outcrossing systems are the evolutionary default state, and many species display these traits, including Arabidopsis lyrata. In contrast to A. lyrata, closely related Arabidopsis thaliana has lost these self-pollen traits and thus represents an excellent system to test genes for reconstructing these evolutionary traits. We previously demonstrated that the ARC1 E3 ligase is required for self-incompatibility in two diverse Brassicaceae species, Brassica napus and A. lyrata, and is frequently deleted in self-compatible species, including A. thaliana. In this study, we examined ARC1's requirement for reconstituting self-incompatibility in A. thaliana and uncovered an important role for ARC1 in promoting a strong and stable pollen rejection response when expressed with two other A. lyrata self-incompatibility factors. Furthermore, we discovered that ARC1 promoted an approach herkogamous phenotype in A. thaliana flowers. Thus, ARC1's expression resulted in two different A. lyrata traits for self-pollen avoidance and highlights the key role that ARC1 plays in the evolution and retention of outcrossing systems.

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Section: Discussionmentioning

confidence: 99%

“…n = 10 for each line (where two stigmatic papillae per stigma for five stigmas were examined). resulting from SRKb expression in the mutant rdr6 background (Tantikanjana et al, 2009). …”

Section: Discussionmentioning

confidence: 99%

The ARC1 E3 Ligase Promotes Two Different Self-Pollen Avoidance Traits inArabidopsis

2014

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“…Col(Sb) stigmas display an intense SI response only in stage 12 floral buds and early stage 13 flowers, but subsequently exhibit breakdown of SI in older flowers (after stage 13) (3). As previously described (3,6), stage 14 Col(Sb) stigmas allowed the growth of numerous SCRb-pollen tubes that penetrated the wall of stigma epidermal cells (Fig. 1B).…”

Section: Resultsmentioning

confidence: 98%

“…As a result, ago7 mutants exhibit up-regulation of the TAS3 ta-siRNA targets Auxin Response Factors 3 and 4 (ARF3 and ARF4) (9-11), which belong to a family of genes encoding DNA-binding proteins that bind to auxin response elements in the promoters of auxin responsive genes (12). We had previously shown that ago7 plants exhibit enhanced SI and stigma exsertion phenotypes similar to those observed in rdr6 plants (6). These results suggested that positive regulators or effectors of SI and pistil development are regulated by ta-siRNA(s) and that ARF3 and/or ARF4 might function in SI.…”

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confidence: 99%

“…In contrast, SRK-SCR transformants of other accessions, such as Col-0, express transient SI, whereby stigmas display an intense SI response only in mature floral buds and justopened flowers, but subsequently exhibit breakdown of SI in older flowers, resulting in abundant seed production (3,4). Using Col-0 plants transformed with the SRKb-SCRb gene pair isolated from the A. lyrata Sb haplotype, henceforth referred to as Col(Sb), we previously demonstrated that a mutation in the RNA-DE-PENDENT RNA POLYMERASE 6 (RDR6) gene drastically reduces self-seed production by enhancing two distinct floral characters that promote outcrossing, SI, and stigma exsertion (i.e., stigmas positioned above the anthers) resulting from enhanced pistil elongation in mature flowers (6).…”

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Non-cell-autonomous regulation of crucifer self-incompatibility by Auxin Response Factor ARF3

Tantikanjana

Nasrallah

2012

Proc. Natl. Acad. Sci. U.S.A.

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In many angiosperms, outcrossing is enforced by genetic selfincompatibility (SI), which allows cells of the pistil to recognize and specifically inhibit "self" pollen. SI is often associated with increased stigma-anther separation, a morphological trait that promotes crosspollen deposition on the stigma. However, the gene networks responsible for coordinate evolution of these complex outbreeding devices are not known. In self-incompatible members of the Brassicaceae (crucifers), the inhibition of "self"-pollen is triggered within the stigma epidermal cell by allele-specific interaction between two highly polymorphic proteins, the stigma-expressed S-locus receptor kinase (SRK) and its pollen coat-localized ligand, the S-locus cysteinerich (SCR) protein. Using Arabidopsis thaliana plants that express SI as a result of transformation with a functional SRK-SCR gene pair, we identify Auxin Response Factor 3 (ARF3) as a mediator of crosstalk between SI signaling and pistil development. We show that ARF3, a regulator of pistil development that is expressed in the vascular tissue of the style, acts non-cell-autonomously to enhance the SI response and simultaneously down-regulate auxin responses in stigma epidermal cells, likely by regulating a mobile signal derived from the stylar vasculature. The inverse correlation we observed in stigma epidermal cells between the strength of SI and the levels of auxin inferred from activity of the auxin-responsive reporter DR5:: GUS suggests that the dampening of auxin responses in the stigma epidermis promotes inhibition of "self" pollen in crucifer SI.pollen-stigma interaction | receptor signaling | auxin signaling | cell-cell communication F lowering plants having both female and male reproductive structures within the same flower have evolved a variety of mechanisms that promote cross-pollination, thereby allowing them to avoid inbreeding depression and maintain genetic variation among individuals. Among the most recognized outcrossing mechanisms are physiological self-incompatibility (SI) systems, which enable cells of the female reproductive tract to recognize and reject genetically related pollen grains, and morphological adaptations in flower architecture that increase the separation between stigma and anther heights and thus minimize the chance of physical contact between pollen and stigma within a flower (1, 2). Although these physiological and morphological barriers to selfing appear to be unrelated mechanistically, they are often found to coevolve, suggesting that SI and floral developmental programs are based on intersecting genetic networks.Arabidopsis thaliana is a highly self-fertile species that harbors nonfunctional alleles of the two genes that determine specificity in the SI response of the Brassicaceae: SRK, which encodes the S-locus receptor kinase (SRK), a transmembrane protein displayed on the surface of stigma epidermal cells, and SCR, which encodes the Slocus cysteine-rich protein, which is the pollen coat-localized ligand for SRK. In previous studies, we sh...

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Trait Transitions in Explicit Ecological and Genomic Contexts: Plant Mating Systems as Case Studies

Castric

Billiard

Vekemans

2013

Advances in Experimental Medicine and Biology

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Plants are astonishingly diverse in how they reproduce sexually, and the study of plant mating systems provides some of the most compelling cases of parallel and independent evolutionary transitions. In this chapter, we review how the massive amount of genomic data being produced is allowing long-standing predictions from ecological and evolutionary theory to be put to test. After a review of theoretical predictions about the importance of considering the genomic architecture of the mating system, we focus on a set of recent discoveries on how the mating system is controlled in a variety of model and non-model species. In parallel, genomic approaches have revealed the complex interaction between the evolution of genes controlling mating systems and genome evolution, both genome-wide and in the mating system control region. In several cases, major transitions in the mating system can be clearly associated with important ecological changes, hence illuminating an important interplay between ecological and genomic approaches. We also list a number of major unsolved questions that remain for the field, and highlight foreseeable conceptual developments that are likely to play a major role in our understanding of how plant mating systems evolve in Nature.

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A Dual Role for the S-Locus Receptor Kinase in Self-Incompatibility and Pistil Development Revealed by an Arabidopsis rdr6 Mutation

Cited by 49 publications

References 53 publications

The ARC1 E3 Ligase Promotes Two Different Self-Pollen Avoidance Traits inArabidopsis

The ARC1 E3 Ligase Promotes Two Different Self-Pollen Avoidance Traits inArabidopsis

Non-cell-autonomous regulation of crucifer self-incompatibility by Auxin Response Factor ARF3

Trait Transitions in Explicit Ecological and Genomic Contexts: Plant Mating Systems as Case Studies

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