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

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. 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.

SUBMITTER: Therezan R

PROVIDER: S-EPMC8222033 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: Many highly beneficial traits (e.g. disease or abiotic stress resistance) have been transferred into crops through crosses with their wild relatives. The 13 recognized species of tomato (Solanum section Lycopersicon) are closely related to each other and wild species genes have been extensively used for improvement of the crop, Solanum lycopersicum L. In addition, the lack of geographical barriers has permitted natural hybridization between S. lycopersicum and its closest wild relative Solanum pimpinellifolium in Ecuador, Peru and northern Chile. In order to better understand patterns of S. lycopersicum diversity, we sequenced 47 markers ranging in length from 130 to 1200?bp (total of 24?kb) in genotypes of S. lycopersicum and wild tomato species S. pimpinellifolium, Solanum arcanum, Solanum peruvianum, Solanum pennellii and Solanum habrochaites. Between six and twelve genotypes were comparatively analyzed per marker. Several of the markers had previously been hypothesized as carrying wild species alleles within S. lycopersicum, i.e., cryptic introgressions. RESULTS: Each marker was mapped with high confidence (e<1 x 10-30) to a single genomic location using BLASTN against tomato whole genome shotgun chromosomes (SL2.40) database. Neighbor-joining trees showed high mean bootstrap support (86.8 ± 2.34%) for distinguishing red-fruited from green-fruited taxa for 38 of the markers. Hybridization and parsimony splits networks, genomic map positions of markers relative to documented introgressions, and historical origins of accessions were used to interpret evolutionary patterns at nine markers with putatively introgressed alleles. CONCLUSION: Of the 47 genetic markers surveyed in this study, four were involved in linkage drag on chromosome 9 during introgression breeding, while alleles at five markers apparently originated from natural hybridization with S. pimpinellifolium and were associated with primitive genotypes of S. lycopersicum. The positive identification of introgressed genes within crop species such as S. lycopersicum will help inform conservation and utilization of crop germplasm diversity, for example, facilitating the purging of undesirable linkage drag or the exploitation of novel, favorable alleles.

Project description:BackgroundMicroRNA319 (miR319) acts as an essential regulator of gene expression during plant development and under stress conditions. Although the role of miR319a in regulating leaf development has been well studied in tomato (Solanum lycopersicum), the function of the recently discovered wild tomato Solanum habrochaites miRNA319d (sha-miR319d) remains poorly understood. In this study, we overexpressed sha-miR319d in cultivated tomato 'Micro-Tom' to further investigate its role in tomato temperature stress responses.ResultsUnder chilling or heat stress, sha-miR319d-overexpressing plants showed enhanced stress tolerance, including lower relative electrolyte leakage (REL), malondialdehyde (MDA) concentration, O2- generation and H2O2 concentration and higher chlorophyll contents and Fv/Fm values than wild-type (WT) plants. Overexpression of sha-miR319d enhanced the activities of superoxide dismutase (SOD) and catalase (CAT), with possible correlation with elevated expression levels of the genes FeSOD, CuZnSOD and CAT. Moreover, different expression levels of key genes involved in chilling (MYB83 and CBF1), heat (HsfA1a, HsfA1b and Hsp90), and reactive oxygen species (ROS) (ZAT12 and ZAT10) signaling in transgenic plants and WT were determined, suggesting a role for sha-miR319d in regulating tomato temperature stress via chilling, heat and ROS signaling. Silencing GAMYB-like1 increased tomato chilling tolerance as well as the expression levels of CBF1, CuZnSOD, CAT, APX1, APX2, ZAT12 and ZAT10. Additionally, overexpression of sha-miR319d in tomato caused plant leaf crinkling and reduced height.ConclusionsOverexpression of sha-miR319d confers chilling and heat stress tolerance in tomato. Sha-miR319d regulates tomato chilling tolerance, possibly by inhibiting expression of GAMYB-like1 and further alters chilling, heat and ROS signal transduction. Our research provides insight for further study of the role of sha-miR319d in tomato growth and stress regulation and lays a foundation for the genetic improvement of tomato.

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

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