scholarly journals A Cysteine-Rich Protein, SpDIR1L, Implicated in S-RNase-Independent Pollen Rejection in the Tomato (Solanum Section Lycopersicon) Clade

2021 ◽  
Vol 22 (23) ◽  
pp. 13067
Author(s):  
Juan Vicente Muñoz-Sanz ◽  
Alejandro Tovar-Méndez ◽  
Lu Lu ◽  
Ru Dai ◽  
Bruce McClure

Tomato clade species (Solanum sect. Lycopersicon) display multiple interspecific reproductive barriers (IRBs). Some IRBs conform to the SI x SC rule, which describes unilateral incompatibility (UI) where pollen from SC species is rejected on SI species’ pistils, but reciprocal pollinations are successful. However, SC x SC UI also exists, offering opportunities to identify factors that contribute to S-RNase-independent IRBs. For instance, SC Solanum pennellii LA0716 pistils only permit SC Solanum lycopersicum pollen tubes to penetrate to the top third of the pistil, while S. pennellii pollen penetrates to S. lycopersicum ovaries. We identified candidate S. pennellii LA0716 pistil barrier genes based on expression profiles and published results. CRISPR/Cas9 mutants were created in eight candidate genes, and mutants were assessed for changes in S. lycopersicum pollen tube growth. Mutants in a gene designated Defective in Induced Resistance 1-like (SpDIR1L), which encodes a small cysteine-rich protein, permitted S. lycopersicum pollen tubes to grow to the bottom third of the style. We show that SpDIR1L protein accumulation correlates with IRB strength and that species with weak or no IRBs toward S. lycopersicum pollen share a 150 bp deletion in the upstream region of SpDIR1L. These results suggest that SpDIR1L contributes to an S-RNase-independent IRB.

2019 ◽  
Author(s):  
Cathleen P Jewell ◽  
Simo Zhang ◽  
Matthew J. S. Gibson ◽  
Alejandro Tovar-Méndez ◽  
Bruce McClure ◽  
...  

AbstractA goal of speciation genetics is to understand how the genetic components underlying interspecific reproductive barriers originate within species. Unilateral incompatibility (UI) is a postmating prezygotic barrier in which pollen rejection in the female reproductive tract (style) occurs in only one direction of an interspecific cross. Natural variation in the strength of UI has been observed among populations within species in the wild tomato clade. In some cases, molecular loci underlying self-incompatibility (SI) are associated with this variation in UI, but the mechanistic connection between these intra- and inter-specific pollen rejection behaviors is poorly understood in most instances. We generated an F2 population between SI and SC genotypes of a single species, Solanum pennellii, to examine the genetic basis of intraspecific variation in the strength of UI against other species, and to determine whether loci underlying SI are genetically associated with this variation. We found that F2 individuals vary in the rate at which UI rejection occurs. One large effect QTL detected for this trait co-localized with the SI-determining S-locus. Moreover, individuals that expressed S-RNase—the S-locus protein involved in SI pollen rejection—in their styles had much more rapid UI responses compared to those without S-RNase protein. Our analysis shows that intraspecific variation at mate choice loci—in this case at loci that prevent self-fertilization—can contribute to variation in the strength of interspecific isolation, including postmating prezygotic barriers. Understanding the nature of such standing variation can provide insight into the accumulation of these barriers between diverging lineages.


2020 ◽  
Vol 111 (2) ◽  
pp. 216-226
Author(s):  
Cathleen P Jewell ◽  
Simo V Zhang ◽  
Matthew J S Gibson ◽  
Alejandro Tovar-Méndez ◽  
Bruce McClure ◽  
...  

Abstract A goal of speciation genetics is to understand how the genetic components underlying interspecific reproductive barriers originate within species. Unilateral incompatibility (UI) is a postmating prezygotic barrier in which pollen rejection in the female reproductive tract (style) occurs in only one direction of an interspecific cross. Natural variation in the strength of UI has been observed among populations within species in the wild tomato clade. In some cases, molecular loci underlying self-incompatibility (SI) are associated with this variation in UI, but the mechanistic connection between these intra- and inter-specific pollen rejection behaviors is poorly understood in most instances. We generated an F2 population between SI and SC genotypes of a single species, Solanum pennellii, to examine the genetic basis of intraspecific variation in UI against other species, and to determine whether loci underlying SI are genetically associated with this variation. We found that F2 individuals vary in the rate at which UI rejection occurs. One large effect QTL detected for this trait co-localized with the SI-determining S-locus. Moreover, individuals that expressed S-RNase—the S-locus protein involved in SI pollen rejection—in their styles had much more rapid UI responses compared with those without S-RNase protein. Our analysis shows that intraspecific variation at mate choice loci—in this case at loci that prevent self-fertilization—can contribute to variation in the expression of interspecific isolation, including postmating prezygotic barriers. Understanding the nature of such intraspecific variation can provide insight into the accumulation of these barriers between diverging lineages.


2021 ◽  
Vol 72 (1) ◽  
pp. 615-639
Author(s):  
Amanda K. Broz ◽  
Patricia A. Bedinger

Pollen-pistil interactions serve as important prezygotic reproductive barriers that play a critical role in mate selection in plants. Here, we highlight recent progress toward understanding the molecular basis of pollen-pistil interactions as reproductive isolating barriers. These barriers can be active systems of pollen rejection, or they can result from a mismatch of required male and female factors. In some cases, the barriers are mechanistically linked to self-incompatibility systems, while others represent completely independent processes. Pollen-pistil reproductive barriers can act as soon as pollen is deposited on a stigma, where penetration of heterospecific pollen tubes is blocked by the stigma papillae. As pollen tubes extend, the female transmitting tissue can selectively limit growth by producing cell wall–modifying enzymes and cytotoxins that interact with the growing pollen tube. At ovules, differential pollen tube attraction and inhibition of sperm cell release can act as barriers to heterospecific pollen tubes.


2017 ◽  
Vol 7 (7) ◽  
pp. 2151-2159 ◽  
Author(s):  
Jennafer A P Hamlin ◽  
Natasha A Sherman ◽  
Leonie C Moyle

Abstract Recognition and rejection of heterospecific male gametes occurs in a broad range of taxa, although the complexity of mechanisms underlying these components of postmating cryptic female choice is poorly understood. In plants, the arena for postmating interactions is the female reproductive tract (pistil), within which heterospecific pollen tube growth can be arrested via active molecular recognition and rejection. Unilateral incompatibility (UI) is one such postmating barrier in which pollen arrest occurs in only one direction of an interspecific cross. We investigated the genetic basis of pistil-side UI between Solanum species, with the specific goal of understanding the role and magnitude of epistasis between UI QTL. Using heterospecific introgression lines (ILs) between Solanum pennellii and S. lycopersicum, we assessed the individual and pairwise effects of three chromosomal regions (ui1.1, ui3.1, and ui12.1) previously associated with interspecific UI among Solanum species. Specifically, we generated double introgression (‘pyramided’) genotypes that combined ui12.1 with each of ui1.1 and ui3.1, and assessed the strength of UI pollen rejection in the pyramided lines, compared to single introgression genotypes. We found that none of the three QTL individually showed UI rejection phenotypes, but lines combining ui3.1 and ui12.1 showed significant pistil-side pollen rejection. Furthermore, double ILs (DILs) that combined different chromosomal regions overlapping ui3.1 differed significantly in their rate of UI, consistent with at least two genetic factors on chromosome three contributing quantitatively to interspecific pollen rejection. Together, our data indicate that loci on both chromosomes 3 and 12 are jointly required for the expression of UI between S. pennellii and S. lycopersicum, suggesting that coordinated molecular interactions among a relatively few loci underlie the expression of this postmating prezygotic barrier. In addition, in conjunction with previous data, at least one of these loci appears to also contribute to conspecific self-incompatibility (SI), consistent with a partially shared genetic basis between inter- and intraspecific mechanisms of postmating prezygotic female choice.


1993 ◽  
Vol 71 (2) ◽  
pp. 353-358 ◽  
Author(s):  
Lawrence D. Harder ◽  
Mitchell B. Cruzan ◽  
James D. Thomson

To determine whether interspecific pollen transfer could reduce seed production by two sympatric lilies, Erythronium albidum and Erythronium americanum, we hand-pollinated flowers with mixtures of conspecific and heterospecific pollen. These species exhibited typical unilateral interspecific incompatibility, i.e., pollen tubes from the self-infertile species (E. americanum) grew apparently unimpeded in styles of the self-fertile species (E. albidum), whereas the reverse cross resulted in an incompatibility reaction. Because of this asymmetrical relation and faster growth by heterospecific pollen tubes in E. albidum stigmas than by conspecific tubes, pollination with abundant heterospecific pollen reduced fruit and seed production by E. albidum, but not by E. americanum, as long as the stigma also received some conspecific pollen. Unilateral incompatibility could benefit self-infertile species in reproductive interactions with closely related self-fertile species; however, this benefit remains to be demonstrated for naturally pollinated plants. Key words: Erythronium albidum, Erythronium americanum, interspecific pollen transfer, pollination, unilateral incompatibility.


2009 ◽  
Vol 2009 ◽  
pp. 1-23 ◽  
Author(s):  
Boryana S. Stamova ◽  
Debbie Laudencia-Chingcuanco ◽  
Diane M. Beckles

The expression of genes involved in starch synthesis in wheat was analyzed together with the accumulation profiles of soluble sugars, starch, protein, and starch granule distribution in developing caryopses obtained from the same biological materials used for profiling of gene expression using DNA microarrays. Multiple expression patterns were detected for the different starch biosynthetic gene isoforms, suggesting their relative importance through caryopsis development. Members of the ADP-glucose pyrophosphorylase, starch synthase, starch branching enzyme, and sucrose synthase gene families showed different expression profiles; expression of some members of these gene families coincided with a period of high accumulation of starch while others did not. A biphasic pattern was observed in the rates of starch and protein accumulation which paralleled changes in global gene expression. Metabolic and regulatory genes that show a pattern of expression similar to starch accumulation and granule size distribution were identified, suggesting their coinvolvement in these biological processes.


2016 ◽  
Author(s):  
Jennafer A. P. Hamlin ◽  
Natasha A. Sherman ◽  
Leonie C. Moyle

ABSTRACTRecognition and rejection of heterospecific male gametes occurs in a broad range of taxa, although the complexity and redundancy of mechanisms underlying this postmating cryptic female choice is poorly understood. In plants, the arena for these interactions is the female reproductive tract (pistil), within which heterospecific pollen tube growth can be arrested via active molecular recognition. Unilateral incompatibility (UI) is one such pistil-mediated barrier in which pollen rejection occurs in only one direction of an interspecific cross. We investigated the genetic basis of pistil-side UI between Solanum species, with the specific goal of understanding the role and magnitude of epistasis between UI QTL. Using heterospecific introgression lines (ILs) between Solanum pennellii and S. lycopersicum, we assessed the individual and pairwise effects of three chromosomal regions (ui1.1, ui3.1, and ui12.1) previously associated with interspecific UI among Solanum species. Specifically, we pyramided ui12.1 with each of ui1.1 and ui3.1, and assessed the strength of UI pollen rejection in pyramided (double introgression) lines, compared to single introgression genotypes. We found that none of the three QTL individually showed UI rejection phenotypes, but lines combining ui3.1 and ui12.1 showed significant pistil-side pollen rejection. Furthermore, double introgression lines that combined different chromosomal regions overlapping ui3.1 differed significantly in their rate of UI, consistent with at least two genetic factors on chromosome three contributing quantitatively to interspecific pollen rejection. Together, our data indicate that loci on both chromosomes 3 and 12 are jointly required for the expression of UI between S. pennellii and S. lycopersicum suggesting that coordinated molecular interactions among a relatively few loci underlying the expression of this postmating prezygotic barrier. In addition, in conjunction with previous data, at least one of these loci appears to also contribute to conspecific self-incompatibility, consistent with a partially shared genetic basis between inter- and intraspecific mechanisms of postmating prezygotic female choice.


Biomolecules ◽  
2019 ◽  
Vol 9 (12) ◽  
pp. 763 ◽  
Author(s):  
Luzhao Pan ◽  
Qinwei Guo ◽  
Songlin Chai ◽  
Yuan Cheng ◽  
Meiying Ruan ◽  
...  

The invertase gene family in plants is composed of two subfamilies of enzymes, namely, acid- and neutral/alkaline invertases (cytosolic invertase, CIN). Both can irreversibly cleave sucrose into fructose and glucose, which are thought to play key roles in carbon metabolism and plant growth. CINs are widely found in plants, but little is reported about this family. In this paper, a comparative genomic approach was used to analyze the CIN gene family in Solanum, including Solanum tuberosum, Solanum lycopersicum, Solanum pennellii, Solanum pimpinellifolium, and Solanum melongena. A total of 40 CINs were identified in five Solanum plants, and sequence features, phylogenetic relationships, motif compositions, gene structure, collinear relationship, and expression profile were further analyzed. Sequence analysis revealed a remarkable conservation of CINs in sequence length, gene number, and molecular weight. The previously verified four amino acid residues (D188, E414, Arg430, and Ser547) were also observed in 39 out of 40 CINs in our study, showing to be deeply conserved. The CIN gene family could be distinguished into groups α and β, and α is further subdivided into subgroups α1 and α2 in our phylogenetic tree. More remarkably, each species has an average of four CINs in the α and β groups. Marked interspecies conservation and collinearity of CINs were also further revealed by chromosome mapping. Exon–intron configuration and conserved motifs were consistent in each of these α and β groups on the basis of in silico analysis. Expression analysis indicated that CINs were constitutively expressed and share similar expression profiles in all tested samples from S. tuberosum and S. lycopersicum. In addition, in CIN genes of the tomato and potato in response to abiotic and biotic stresses, phytohormones also performed. Overall, CINs in Solanum were encoded by a small and highly conserved gene family, possibly reflecting structural and functional conservation in Solanum. These results lay the foundation for further expounding the functional characterization of CIN genes and are also significant for understanding the evolutionary profiling of the CIN gene family in Solanum.


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