Novel Sources of Resistance to Fusarium oxysporum f. sp. lycopersici Race 3 Among Solanum pennellii Accessions

Fusarium wilt of tomato (Solanum lycopersicum), caused by fungal pathogen Fusarium oxysporum f. sp. lycopersici (Fol), is one of the most important diseases in tomato production. Three races of the pathogen are described, and race-specific resistance genes have been applied in commercial tomato cultivars for controlling the disease. Race 3 (Fol3) threatens tomato production in many regions around the world, and novel resistance resources could expand the diversity and durability of Fol resistance. The wild tomato species, Solanum pennellii, is reported to harbor broad resistance to Fol and was the source of two known Fol3 resistance genes. In this study, we evaluated 42 S. pennellii accessions for resistance to each fusarium wilt race. F1 plants, developed from crossing each accession with the Fol3 susceptible line ‘Suncoast’, were evaluated for Fol3 resistance, and BC1F1 plants were screened to determine the likelihood that Fol3 resistance was based on a novel locus (loci). Nearly all accessions showed resistance to Fol3, and many accessions were resistant to all races. Evaluation of F1 plants indicated a dominant resistance effect to Fol3 from most accessions. Genetic analysis indicated 24 accessions are expected to contain one or more novel Fol3 resistance loci other than an allele near the I-3 locus. To investigate genetic structure of the S. pennellii accessions used in this study, we genotyped all 42 accessions using genotyping by sequencing. Approximately 20% of the single nucleotide polymorphism (SNP) loci were heterozygous across accessions, likely due to the outcrossing nature of the species. Genetic structure analysis at 49,120 unique SNP loci across accessions identified small but obvious genetic differentiations.

Edaphoclimatic Descriptors of Wild Tomato Species (Solanum Sect. Lycopersicon) and Closely Related Species (Solanum Sect. Juglandifolia and Sect. Lycopersicoides) in South America

Wild species related to cultivated tomato are essential genetic resources in breeding programs focused on food security to face future challenges. The ecogeographic analysis allows identifying the species adaptive ranges and most relevant environmental variables explaining their patterns of actual distribution. The objective of this research was to identify the diversity, ecological descriptors, and statistical relationship of 35 edaphoclimatic variables (20 climatic, 1 geographic and 14 edaphic variables) from 4,649 accessions of 12 wild tomato species and 4 closely related species classified in Solanum sect. Lycopersicon and clustered into four phylogenetic groups, namely “Lycopersicon group” (S. pimpinellifolium, S. cheesmaniae, and S. galapagense), “Arcanum group” (S. arcanum, S. chmielewskii, and S. neorickii), “Eriopersicon group” (S. habrochaites, S. huaylasense, S. corneliomulleri, S. peruvianum, and S. chilense), “Neolycopersicon group” (S. pennellii); and two phylogenetically related groups in Solanum sect. Juglandifolia (S. juglandifolium and S. ochranthum), and section Lycopersicoides (S. lycopersicoides and S. sitiens). The relationship between the climate and edaphic variables were determined by the canonical correlation analysis, reaching 89.2% of variation with the first three canonical correlations. The most significant climatic variables were related to humidity (annual evapotranspiration, annual precipitation, and precipitation of driest month) and physicochemical soil characteristics (bulk density, pH, and base saturation percentage). In all groups, ecological descriptors and diversity patterns were consistent with previous reports. Regarding edaphoclimatic diversity, 12 climate types and 17 soil units were identified among all species. This approach has promissory applications for biodiversity conservation and uses valuable genetic resources related to a leading crop.

The Sm Gene Conferring Resistance to Gray Leaf Spot Disease Encodes a NBS-LRR Plant Resistance Protein in Tomato

Gray leaf spot (GLS), caused by Stemphylium lycopersici (S. lycopersici), is one of the most devastating diseases in tomato (Solanum lycopersicum). The resistance (R) gene, Sm, conferring high resistance to S. lycopersici, was introgressed into cultivated tomatoes from the wild tomato species Solanum pimpinellifolium (S. pimpinellifolium). Recently, several studies reported the mapping of the Sm gene. To date, however, it has not been cloned yet. Here, we cloned this resistance gene using a map-based cloning strategy. The Sm gene was mapped in a 160 kb interval of Chromosome 11 between two markers, M390 and M410, by using an F2 population from a cross between the resistant cultivar ‘Motelle’ (Mt) and susceptible line ‘Moneymaker’ (Mm). Three clustered NBS-LRR resistance genes, Solyc11g020080 (R1), Solyc11g020090 (R2) and Solyc11g020100 (R3) were identified in this interval. Nonsynonymous SNPs were identified only in the ORF of R3, supporting it may be a strong candidate gene for Sm. Furthermore, gene silencing of R3 abolished the high resistance to S. lycopersici in Motelle, demonstrating that it is the gene that confers high resistance to S. lycopersici. The clone of Sm gene will provide new opportunities for innovative breeding strategies to breed multi-resistant tomato cultivars.

Characterization of 15-cis-ζ-Carotene Isomerase Z-ISO in Cultivated and Wild Tomato Species Differing in Ripe Fruit Pigmentation

Isomerization of 9,15,9′-tri-cis-ζ-carotene mediated by 15-cis-ζ-carotene isomerase Z-ISO is a critical step in the biosynthesis of carotenoids, which define fruit color. The tomato clade (Solanum section Lycopersicon) comprises the cultivated tomato (Solanum lycopersicum) and 12 related wild species differing in fruit color and, thus, represents a good model for studying carotenogenesis in fleshy fruit. In this study, we identified homologous Z-ISO genes, including 5′-UTRs and promoter regions, in 12 S. lycopersicum cultivars and 5 wild tomato species (red-fruited Solanum pimpinellifolium, yellow-fruited Solanum cheesmaniae, and green-fruited Solanum chilense, Solanum habrochaites, and Solanum pennellii). Z-ISO homologs had a highly conserved structure, suggesting that Z-ISO performs a similar function in tomato species despite the difference in their fruit color. Z-ISO transcription levels positively correlated with the carotenoid content in ripe fruit of the tomatoes. An analysis of the Z-ISO promoter and 5′-UTR sequences revealed over 130 cis-regulatory elements involved in response to light, stresses, and hormones, and in the binding of transcription factors. Green- and red/yellow-fruited Solanum species differed in the number and position of cis-elements, indicating changes in the transcriptional regulation of Z-ISO expression during tomato evolution, which likely contribute to the difference in fruit color.

Comparative RNA-Seq Analysis Reveals Potentially Resistance-Related Genes in Response to Bacterial Canker of Tomato

Tomato is one of the most important crops for human consumption. Its production is affected by the actinomycete Clavibacter michiganensis subsp. michiganensis (Cmm), one of the most devastating bacterial pathogens of this crop. Several wild tomato species represent a source of natural resistance to Cmm. Here, we contrasted the transcriptomes of the resistant wild tomato species Solanum arcanum LA2157 and the susceptible species Solanum lycopersicum cv. Ailsa Craig, during the first 24 h of challenge with Cmm. We used three analyses approaches which demonstrated to be complementary: mapping to S. lycopersicum reference genome SL3.0; semi de novo transcriptome assembly; and de novo transcriptome assembly. In a global context, transcriptional changes seem to be similar between both species, although there are some specific genes only upregulated in S. arcanum during Cmm interaction, suggesting that the resistance regulatory mechanism probably diverged during the domestication process. Although S. lycopersicum showed enriched functional groups related to defense, S. arcanum displayed a higher number of induced genes related to bacterial, oomycete, and fungal defense at the first few hours of interaction. This study revealed genes that may contribute to the resistance phenotype in the wild tomato species, such as those that encode for a polyphenol oxidase E, diacyl glycerol kinase, TOM1-like protein 6, and an ankyrin repeat-containing protein, among others. This work will contribute to a better understanding of the defense mechanism against Cmm, and the development of new control methods.

Development of biotic stress resistant F1 interspecific hybrid rootstock derived from Solanum lycopersicum and Solanum habrochaites

Tomato is major horticultural plant consumed worldwide. Biotic stress (nematodes, fungus and bacteria) has negative effect on tomato production due to causing reduced yield or plant death. Rootstocks confer resistance to soil-borne pathogen are considered the most effective and environment friendly approach for such a stress management. Thus, development of genetic resources having multiple resistance genes is essential for sustainable tomato breeding. Solanum habrochaites is one of the most studied wild tomato species due to its high genetic potential for biotic and abiotic stresses. In the present study, rootstock potential of an interspecific F1 hybrid derived from S. habrochaites was evaluated as using resistance genes (Frl, I-2, I-3, Mi-3, Pto Ty-1, Ty-3 and Sw-5) specific molecular markers for 6 major tomato diseases and 31 fruit quality traits. The study reported that F1 hybrid had resistance alleles for 5 genes (Frl, I-2, I-3, Pto and Sw-5) confer resistance to fusarium crown rot disease, crown – root rot disease, race 2 and 3 of Fusarium oxysporum f. sp. radicis lycopersici, bacterial speck and tomato spotted wilt virus (TSWV), respectively. Despite high performance of F1 hybrid for biotic stress, the study pointed S. habrochaites specific graft incompatibility due to poor rate of grafting efficiency, small fruit formation and low yield. This is the first comprehensive study evaluated the horticultural performance of an interspecific hybrid in tomato.

Breeding for Resistance to Fusarium Wilt of Tomato: A Review

For over a century, breeders have worked to develop tomato (Solanum lycopersicum) cultivars with resistance to Fusarium wilt (Fol) caused by the soilborne fungus Fusarium oxysporum f. sp. lycopersici. Host resistance is the most effective strategy for the management of this disease. For each of the three Fol races, resistance has been introgressed from wild tomato species, predominately in the form of R genes. The I, I-2, I-3, and I-7 R genes have each been identified, as well as the corresponding Avr effectors in the fungus with the exception of Avr7. The mechanisms by which the R gene protein products recognize these effectors, however, has not been elucidated. Extensive genetic mapping, gene cloning, and genome sequencing efforts support the development of tightly-linked molecular markers, which greatly expedite tomato breeding and the development of elite, Fol resistant cultivars. These resources also provide important tools for pyramiding resistance genes and should support the durability of host resistance.

Tomato leaves under stress: a comparison of stress response to mild abiotic stress between a cultivated and a wild tomato species

Tomato is one of the most produced crop plants on earth and growing in the fields and greenhouses all over the world. Breeding with known traits of wild species can enhance stress tolerance of cultivated crops. In this study, we investigated responses of the transcriptome as well as primary and secondary metabolites in leaves of a cultivated and a wild tomato to several abiotic stresses such as nitrogen deficiency, chilling or warmer temperatures, elevated light intensities and combinations thereof. The wild species responded different to varied temperature conditions compared to the cultivated tomato. Nitrogen deficiency caused the strongest responses and induced in particular the secondary metabolism in both species but to much higher extent in the cultivated tomato. Our study supports the potential of a targeted induction of valuable secondary metabolites in green residues of horticultural production, that will otherwise only be composted after fruit harvest. In particular, the cultivated tomato showed a strong induction in the group of mono caffeoylquinic acids in response to nitrogen deficiency. In addition, the observed differences in stress responses between cultivated and wild tomato can lead to new breeding targets for better stress tolerance.

Local and temporal adaptation to climatic change in a wild tomato species via selective sweeps.

Positive Darwinian selection is the driving force underpinning local (in space) and temporal (in time) adaptation, and leaves footprints of selective sweeps at the underlying major genes. These two adaptive processes are classically considered independently, so that most genomic selection scans uncover only recent sweeps underpinning spatial adaptation. However, understanding if these adaptive processes are intermingled and share common genetic bases is crucial to predict a species evolutionary potential, for example in response to changing environmental conditions. We use whole genome data from six populations across three different habitats of the wild tomato species Solanum chilense, to 1) infer the past demographic history, and 2) search for genes under strong positive selection. We then correlate the demographic history, allele frequencies in space and time, the age of selection events and the reconstructed historical ecological distribution of the species over five main climatic periods spanning 150,000 years. We find evidence for several selective sweeps targeting regulatory networks involved in root hair development in low altitude, and response to photoperiod and vernalization in high altitude populations. These sweeps occur in a concerted fashion in a given regulatory gene network and only at particular time periods, thereby underpinning temporal local adaptation. These genes under positive selection provide subsequently the basis for spatial local adaptation to novel habitats when new ecological niches become available. Our results reveal the importance of jointly studying spatial and temporal adaptations in species during habitat colonization.