scholarly journals Intraspecific genetic variation underlying postmating reproductive barriers between species in the wild tomato clade (Solanum sect. Lycopersicon)

2019 ◽  
Author(s):  
Cathleen P Jewell ◽  
Simo Zhang ◽  
Matthew J. S. Gibson ◽  
Alejandro Tovar-Méndez ◽  
Bruce McClure ◽  
...  
Keyword(s):  
Intraspecific Variation ◽  
Interspecific Cross ◽  
Female Reproductive Tract ◽  
Reproductive Barriers ◽  
Solanum Pennellii ◽  
Wild Tomato ◽  
Genetic Components ◽  
Standing Variation ◽  
Pollen Rejection ◽  
In The Wild

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.

scholarly journals Intraspecific Genetic Variation Underlying Postmating Reproductive Barriers between Species in the Wild Tomato Clade (Solanum sect. Lycopersicon)

2020 ◽  
Vol 111 (2) ◽  
pp. 216-226
Author(s):  
Cathleen P Jewell ◽  
Simo V Zhang ◽  
Matthew J S Gibson ◽  
Alejandro Tovar-Méndez ◽  
Bruce McClure ◽  
...  
Keyword(s):  
Intraspecific Variation ◽  
Interspecific Cross ◽  
Female Reproductive Tract ◽  
Reproductive Barriers ◽  
S Locus ◽  
Solanum Pennellii ◽  
Wild Tomato ◽  
Genetic Components ◽  
Pollen Rejection ◽  
In The Wild

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.

scholarly journals Two Loci Contribute Epistastically to Heterospecific Pollen Rejection, a Postmating Isolating Barrier Between Species

2017 ◽  
Vol 7 (7) ◽  
pp. 2151-2159 ◽  
Author(s):  
Jennafer A P Hamlin ◽  
Natasha A Sherman ◽  
Leonie C Moyle
Keyword(s):  
Female Choice ◽  
Genetic Basis ◽  
Reproductive Tract ◽  
Interspecific Cross ◽  
Solanum Species ◽  
Female Reproductive Tract ◽  
Solanum Pennellii ◽  
Heterospecific Pollen ◽  
Male Gametes ◽  
Pollen Rejection

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.

scholarly journals Two loci contribute epistastically to heterospecific pollen rejection, a postmating isolating barrier between species

2016 ◽  
Author(s):  
Jennafer A. P. Hamlin ◽  
Natasha A. Sherman ◽  
Leonie C. Moyle
Keyword(s):  
Female Choice ◽  
Genetic Basis ◽  
Reproductive Tract ◽  
Interspecific Cross ◽  
Introgression Lines ◽  
Female Reproductive Tract ◽  
Solanum Pennellii ◽  
Heterospecific Pollen ◽  
Male Gametes ◽  
Pollen Rejection

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.

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
Keyword(s):  
Expression Profiles ◽  
Pollen Tubes ◽  
Upstream Region ◽  
Protein Accumulation ◽  
Reproductive Barriers ◽  
Solanum Pennellii ◽  
Unilateral Incompatibility ◽  
Pollen Rejection ◽  
Cysteine Rich Protein ◽  
Solanum Sect

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.

scholarly journals Evolution of metabolic novelty: A trichome-expressed invertase creates specialized metabolic diversity in wild tomato

2019 ◽  
Vol 5 (4) ◽  
pp. eaaw3754 ◽  
Author(s):  
Bryan J. Leong ◽  
Daniel B. Lybrand ◽  
Yann-Ru Lou ◽  
Pengxiang Fan ◽  
Anthony L. Schilmiller ◽  
...  
Keyword(s):  
Biosynthetic Pathway ◽  
Gland Cell ◽  
Metabolic Enzyme ◽  
South American ◽  
Metabolic Diversity ◽  
Solanum Pennellii ◽  
Wild Tomato ◽  
Specialized Metabolites ◽  
New Class ◽  
In The Wild

Plants produce a myriad of taxonomically restricted specialized metabolites. This diversity—and our ability to correlate genotype with phenotype—makes the evolution of these ecologically and medicinally important compounds interesting and experimentally tractable. Trichomes of tomato and other nightshade family plants produce structurally diverse protective compounds termed acylsugars. While cultivated tomato (Solanum lycopersicum) strictly accumulates acylsucroses, the South American wild relative Solanum pennellii produces copious amounts of acylglucoses. Genetic, transgenic, and biochemical dissection of the S. pennellii acylglucose biosynthetic pathway identified a trichome gland cell–expressed invertase-like enzyme that hydrolyzes acylsucroses (Sopen03g040490). This enzyme acts on the pyranose ring–acylated acylsucroses found in the wild tomato but not on the furanose ring–decorated acylsucroses of cultivated tomato. These results show that modification of the core acylsucrose biosynthetic pathway leading to loss of furanose ring acylation set the stage for co-option of a general metabolic enzyme to produce a new class of protective compounds.

scholarly journals Evolution of metabolic novelty: a trichome-expressed invertase creates specialized metabolic diversity in wild tomato

2018 ◽  
Author(s):  
Bryan J. Leong ◽  
Daniel Lybrand ◽  
Yann-Ru Lou ◽  
Pengxiang Fan ◽  
Anthony L. Schilmiller ◽  
...  
Keyword(s):  
Biosynthetic Pathway ◽  
Gland Cell ◽  
Metabolic Enzyme ◽  
South American ◽  
Metabolic Diversity ◽  
Solanum Pennellii ◽  
Wild Tomato ◽  
Specialized Metabolites ◽  
New Class ◽  
In The Wild

AbstractPlants produce myriad taxonomically restricted specialized metabolites. This diversity – and our ability to correlate genotype with phenotype – makes the evolution of these ecologically and medicinally important compounds interesting and experimentally tractable. Trichomes of tomato and other nightshade family plants produce structurally diverse protective compounds termed acylsugars. While cultivated tomato (Solanum lycopersicum) accumulates strictly acylsucroses, the South American wild relative Solanum pennellii produces copious amounts of acylglucoses. Genetic, transgenic and biochemical dissection of the S. pennellii acylglucose biosynthetic pathway identified a trichome gland cell expressed invertase-like enzyme that hydrolyzes acylsucroses (Sopen03g040490). This enzyme acts on the pyranose ring-acylated acylsucroses found in the wild tomato but not the furanose ring-decorated acylsucroses of cultivated tomato. These results show that modification of the core acylsucrose biosynthetic pathway leading to loss of furanose ring acylation set the stage for co-option of a general metabolic enzyme to produce a new class of protective compounds.

scholarly journals Introgression of the sesquiterpene biosynthesis from Solanum habrochaites to cultivated tomato offers insights into trichome morphology and arthropod resistance

Planta ◽  
2021 ◽  
Vol 254 (1) ◽  
Author(s):  
Rodrigo Therezan ◽  
Ruy Kortbeek ◽  
Eloisa Vendemiatti ◽  
Saioa Legarrea ◽  
Severino M. de Alencar ◽  
...  
Keyword(s):  
Glandular Trichomes ◽  
Pest Resistance ◽  
Chromosome 8 ◽  
Cavity Size ◽  
Solanum Habrochaites ◽  
Genetic Components ◽  
Internal Storage ◽  
In The Wild ◽  
Low Levels ◽  
Trichome Morphology

Abstract Main conclusion Cultivated tomatoes harboring the plastid-derived sesquiterpenes from S. habrochaites have altered type-VI trichome morphology and unveil additional genetic components necessary for piercing-sucking pest resistance. Abstract Arthropod resistance in the tomato wild relative Solanum habrochaites LA1777 is linked to specific sesquiterpene biosynthesis. The Sesquiterpene synthase 2 (SsT2) gene cluster on LA1777 chromosome 8 controls plastid-derived sesquiterpene synthesis. The main genes at SsT2 are Z-prenyltransferase (zFPS) and Santalene and Bergamotene Synthase (SBS), which produce α-santalene, β-bergamotene, and α-bergamotene in LA1777 round-shaped type-VI glandular trichomes. Cultivated tomatoes have mushroom-shaped type-VI trichomes with much smaller glands that contain low levels of monoterpenes and cytosolic-derived sesquiterpenes, not presenting the same pest resistance as in LA1777. We successfully transferred zFPS and SBS from LA1777 to cultivated tomato (cv. Micro-Tom, MT) by a backcrossing approach. The trichomes of the MT-Sst2 introgressed line produced high levels of the plastid-derived sesquiterpenes. The type-VI trichome internal storage-cavity size increased in MT-Sst2, probably as an effect of the increased amount of sesquiterpenes, although it was not enough to mimic the round-shaped LA1777 trichomes. The presence of high amounts of plastid-derived sesquiterpenes was also not sufficient to confer resistance to various tomato piercing-sucking pests, indicating that the effect of the sesquiterpenes found in the wild S. habrochaites can be insect specific. Our results provide for a better understanding of the morphology of S. habrochaites type-VI trichomes and paves the way to obtain insect-resistant tomatoes.

scholarly journals Intraspecific variation in symbiont density in an insect-microbe symbiosis

2020 ◽  
Author(s):  
Benjamin J. Parker ◽  
Jan Hrček ◽  
Ailsa H.C. McLean ◽  
Jennifer A. Brisson ◽  
H. Charles J. Godfray
Keyword(s):  
Intraspecific Variation ◽  
Fungal Pathogens ◽  
Acyrthosiphon Pisum ◽  
Natural Populations ◽  
Pea Aphid ◽  
Optimal Density ◽  
Evolutionary Forces ◽  
Standing Variation ◽  
Dramatic Decline

AbstractMany insects host vertically-transmitted microbes, which can confer benefits to their hosts but are costly to maintain and regulate. A key feature of these symbioses is variation: for example, symbiont density can vary among host and symbiont genotypes. However, the evolutionary forces maintaining this variation remain unclear. We studied variation in symbiont density using the pea aphid (Acyrthosiphon pisum) and the bacterium Regiella insecticola, a symbiont that can protect its host against fungal pathogens. We found that relative symbiont density varies both between two Regiella phylogenetic clades and among aphid ‘biotypes’. Higher-density symbiont infections are correlated with stronger survival costs, but variation in density has little effect on the protection Regiella provides against fungus. Instead, we found that in some aphid genotypes, a dramatic decline in symbiont density precedes the loss of a symbiont infection. Together, our data suggest that the optimal density of a symbiont infection is likely different from the perspective of aphid and microbial fitness. Regiella might prevent loss by maintaining high within-host densities, but hosts do not appear to benefit from higher symbiont numbers and may be advantaged by losing costly symbionts in certain environments. The standing variation in symbiont density observed in natural populations could therefore be maintained by antagonistic coevolutionary interactions between hosts and their symbiotic microbes.

scholarly journals Candidate Gene Networks for Acylsugar Metabolism and Plant Defense in Wild Tomato Solanum pennellii

2019 ◽  
Vol 32 (1) ◽  
pp. 81-99 ◽  
Author(s):  
Sabyasachi Mandal ◽  
Wangming Ji ◽  
Thomas D. McKnight
Keyword(s):  
Plant Defense ◽  
Candidate Gene ◽  
Gene Networks ◽  
Solanum Pennellii ◽  
Wild Tomato

scholarly journals Bactericera cockerelli resistance in the wild tomato Solanum habrochaites is polygenic and influenced by the presence of Candidatus Liberibacter solanacearum

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Carlos A. Avila ◽  
Thiago G. Marconi ◽  
Zenaida Viloria ◽  
Julianna Kurpis ◽  
Sonia Y. Del Rio
Keyword(s):  
Recombinant Inbred Lines ◽  
Chromosome 8 ◽  
Bactericera Cockerelli ◽  
Wild Tomato ◽  
Wild Tomato Species ◽  
Tomato Species ◽  
Cultivar Development ◽  
In The Wild ◽  
Candidatus Liberibacter ◽  
Complex Inheritance

Abstract The tomato-potato psyllid (TPP), Bactericera cockerelli, is a vector for the phloem-limited bacterium Candidatus Liberibacter solanacearum (Lso), the causative agent of economically important diseases including tomato vein-greening and potato zebra chip. Here, we screened 11 wild tomato relatives for TPP resistance as potential resources for tomato (Solanum lycopersicum) cultivar development. Six accessions with strong TPP resistance (survival <10%) were identified within S. habrochaites, S. pennelli, S. huaylasense, S. chmielewskii, S. corneliomulleri, and S. galapagense. Two S. pennelli and S. corneliomulleri accessions also showed resistance to Lso. We evaluated recombinant inbred lines (RILs) carrying resistance from S. habrochaites accession LA1777 in the S. lycopersicum background and identified major quantitative trait loci (QTLs) responsible for adult TPP mortality and fecundity in several RILs carrying insertions in different chromosomes, indicating the polygenic nature of these traits. Analysis of a major resistance QTL in RIL LA3952 on chromosome 8 revealed that the presence of Lso is required to increase adult TPP mortality. By contrast, the reduced TPP oviposition trait in LA3952 is independent of Lso. Therefore, resistance traits are available in wild-tomato species, although their complex inheritance and modes of action require further characterisation to optimise their utilisation for tomato improvement.

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