Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits
Background: Tomato mutants altered in leaf morphology are usually identified in the greenhouse, which demands considerable time and space and can only be performed in adequate periods. For a faster but equally reliable scrutiny method we addressed the screening in vitro of 971 T-DNA lines. Leaf deve...
- Autores:
-
Jáquez Gutiérrez, Marybel
Atarés, Alejandro
Pineda, Benito
Angarita Díaz, María del Pilar
Ribelles, Carlos
García Sogo, Begoña
Sánchez López, Jorge
Capel, Carmen
Yuste Lisbona, Fernando
Lozano, Rafael
Moreno, Vicente
- Tipo de recurso:
- Article of journal
- Fecha de publicación:
- 2019
- Institución:
- Universidad Cooperativa de Colombia
- Repositorio:
- Repositorio UCC
- Idioma:
- OAI Identifier:
- oai:repository.ucc.edu.co:20.500.12494/17418
- Acceso en línea:
- https://doi.org/10.1186/s12870-019-1735-9
https://hdl.handle.net/20.500.12494/17418
- Palabra clave:
- Tomato
T-DNA lines
Screening in vitro
Mutants
Leaf development
Organ curvature
- Rights
- openAccess
- License
- Atribución
| id |
COOPER2_06aeb66efebb1c711d8cad4eec0f41bd |
|---|---|
| oai_identifier_str |
oai:repository.ucc.edu.co:20.500.12494/17418 |
| network_acronym_str |
COOPER2 |
| network_name_str |
Repositorio UCC |
| repository_id_str |
|
| dc.title.spa.fl_str_mv |
Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits |
| title |
Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits |
| spellingShingle |
Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits Tomato T-DNA lines Screening in vitro Mutants Leaf development Organ curvature |
| title_short |
Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits |
| title_full |
Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits |
| title_fullStr |
Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits |
| title_full_unstemmed |
Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits |
| title_sort |
Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits |
| dc.creator.fl_str_mv |
Jáquez Gutiérrez, Marybel Atarés, Alejandro Pineda, Benito Angarita Díaz, María del Pilar Ribelles, Carlos García Sogo, Begoña Sánchez López, Jorge Capel, Carmen Yuste Lisbona, Fernando Lozano, Rafael Moreno, Vicente |
| dc.contributor.author.none.fl_str_mv |
Jáquez Gutiérrez, Marybel Atarés, Alejandro Pineda, Benito Angarita Díaz, María del Pilar Ribelles, Carlos García Sogo, Begoña Sánchez López, Jorge Capel, Carmen Yuste Lisbona, Fernando Lozano, Rafael Moreno, Vicente |
| dc.subject.spa.fl_str_mv |
Tomato T-DNA lines Screening in vitro Mutants Leaf development Organ curvature |
| topic |
Tomato T-DNA lines Screening in vitro Mutants Leaf development Organ curvature |
| description |
Background: Tomato mutants altered in leaf morphology are usually identified in the greenhouse, which demands considerable time and space and can only be performed in adequate periods. For a faster but equally reliable scrutiny method we addressed the screening in vitro of 971 T-DNA lines. Leaf development was evaluated in vitro in seedlings and shoot-derived axenic plants. New mutants were characterized in the greenhouse to establish the relationship between in vitro and in vivo leaf morphology, and to shed light on possible links between leaf development and agronomic traits, a promising field in which much remains to be discovered. Results: Following the screening in vitro of tomato T-DNA lines, putative mutants altered in leaf morphology were evaluated in the greenhouse. The comparison of results in both conditions indicated a general phenotypic correspondence, showing that in vitro culture is a reliable system for finding mutants altered in leaf development. Apart from providing homogeneous conditions, the main advantage of screening in vitro lies in the enormous time and space saving. Studies on the association between phenotype and nptII gene expression showed co-segregation in two lines (P > 99%). The use of an enhancer trap also allowed identifying gain-of-function mutants through reporter expression analysis. These studies suggested that genes altered in three other mutants were T-DNA tagged. New mutants putatively altered in brassinosteroid synthesis or perception, mutations determining multiple pleiotropic effects, lines affected in organ curvature, and the first tomato mutant with helical growth were discovered. Results also revealed new possible links between leaf development and agronomic traits, such as axillary branching, flower abscission, fruit development and fruit cracking. Furthermore, we found that the gene tagged in mutant 2635-MM encodes a Sterol 3-beta-glucosyltransferase. Expression analysis suggested that abnormal leaf development might be due to the lack-off-function of this gene. Conclusion: In vitro culture is a quick, efficient and reliable tool for identifying tomato mutants altered in leaf morphology. The characterization of new mutants in vivo revealed new links between leaf development and some agronomic traits. Moreover, the possible implication of a gene encoding a Sterol 3-beta-glucosyltransferase in tomato leaf development is reported. |
| publishDate |
2019 |
| dc.date.issued.none.fl_str_mv |
2019-04-15 |
| dc.date.accessioned.none.fl_str_mv |
2020-04-15T20:21:40Z |
| dc.date.available.none.fl_str_mv |
2020-04-15T20:21:40Z |
| dc.type.none.fl_str_mv |
Artículo |
| dc.type.coar.fl_str_mv |
http://purl.org/coar/resource_type/c_2df8fbb1 |
| dc.type.coar.none.fl_str_mv |
http://purl.org/coar/resource_type/c_6501 |
| dc.type.coarversion.none.fl_str_mv |
http://purl.org/coar/version/c_970fb48d4fbd8a85 |
| dc.type.driver.none.fl_str_mv |
info:eu-repo/semantics/article |
| dc.type.version.none.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
| format |
http://purl.org/coar/resource_type/c_6501 |
| status_str |
publishedVersion |
| dc.identifier.uri.spa.fl_str_mv |
https://doi.org/10.1186/s12870-019-1735-9 |
| dc.identifier.uri.none.fl_str_mv |
https://hdl.handle.net/20.500.12494/17418 |
| dc.identifier.bibliographicCitation.spa.fl_str_mv |
Jáquez Gutiérrez, M., Atarés, A., Pineda, B., Angarita, P., Ribelles, C., García Sogo, B. ... Moreno, V. (2019). Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits. BMC Plant Biol 19, 141. https://doi.org/10.1186/s12870-019-1735-9 |
| url |
https://doi.org/10.1186/s12870-019-1735-9 https://hdl.handle.net/20.500.12494/17418 |
| identifier_str_mv |
Jáquez Gutiérrez, M., Atarés, A., Pineda, B., Angarita, P., Ribelles, C., García Sogo, B. ... Moreno, V. (2019). Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits. BMC Plant Biol 19, 141. https://doi.org/10.1186/s12870-019-1735-9 |
| dc.relation.isversionof.spa.fl_str_mv |
https://link.springer.com/article/10.1186/s12870-019-1735-9 |
| dc.relation.ispartofjournal.spa.fl_str_mv |
BMC Plant Biology |
| dc.relation.references.spa.fl_str_mv |
Li N, Jia J, Xia C, Liu X, Kong X. Characterization and mapping of novel chlorophyll deficient mutant genes in durum wheat. Breed Sci. 2013;63:169–75 Aluru MR, Yu F, Fu AG, Rodermel S. Arabidopsis variegation mutants: new insights into chloroplast biogenesis. J Exp Bot. 2006;57:1871–81. Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E. The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell. 1996;84:735–44 Efroni I, Eshed Y, Lifschitz E. Morphogenesis of simple and compound leaves: a critical review. Plant Cell. 2010;22:1019–32. Gonzalez N, Vanhaeren H, Inze D. Leaf size control: complex coordination of cell division expansion. Trends Plant Sci. 2012;17:332–40. Tsukaya H. Leaf Development, The Arabidopsis Book; 2013. https://doi.org/ 10.1199/tab.0163 Kessler S, Kim M, Pham T, Weber N, Sinha N. Mutations altering leaf morphology in tomato. Int J Plant Sci. 2001;162:475–92. Sarlikioti V, de Visser PHB, Buck-Sorlin GH, Marcelis LFM. How plant architecture affects light absorption and photosynthesis in tomato: towards an ideotype for plant architecture using a functional–structural plant model. Ann Bot. 2011;108:1065–73 Rothan C, Bres C, Garcia V, Just D. Tomato resources for functional genomics. In: Causse M, Giovannoni J, Bouzayen M, Zouine M, editors. The tomato genome. Compendium of plant genomes. Berlin: Springer; 2016. p. 75–94. Menda N, Semel Y, Peled D, Eshed Y, Zamir D. In silico screening of a saturated mutation library of tomato. Plant J. 2004;38:861–72 Meissner R, Jacobson Y, Melamed S, Levyatuv S, Shalev G, Ashri A, Elkind Y, Levy A. A new model system for tomato genetics. Plant J. 1997;12:1465–72. Dan Y, Fei Z, Rothan C. Micro-tom - a new model plant for genomics. Genes Genomes Genomics. 2007;1:167–79. Matsukura C, Yamaguchi I, Inamura M, Ban Y, Kobayashi Y, Yin YG, Saito T, Kuwata C, Imanishi S, Nishimura S. Generation of gamma irradiationinduced mutant lines of the miniature tomato (Solanum lycopersicum L.) cultivar ‘Micro-Tom’. Plant Biotechnol. 2007;24:39–44 Watanabe S, Mizoguchi T, Aoki K, Kubo Y, Mori H, Imanishi S, Yamazaki Y, Shibata D, Ezura H. Ethylmethanesulfonate (EMS) mutagenesis of Solanum lycopercisum cv. Micro-tom for large-scale mutant screens. Plant Biotech. 2007;24:33–8 Minoia S, Petrozza A, D’Onofrio O, Piron F, Mosca G, Sozio G, Cellini F, Bendahmane A, Carriero F. A new mutant genetic resource for tomato crop improvement by TILLING technology. BMC Res Notes. 2010;3:69. Okabe Y, Asamizu E, Saito T, Matsukura C, Ariizumi T, Brès C, Rothan C, Mizoguchi T, Ezura H. Tomato TILLING technology: development of a reverse genetics tool for the efficient isolation of mutants from micro-tom mutant libraries. Plant Cell Physiol. 2011;52:1994–2005. Saito T, Ariizumi T, Okabe Y, Asamizu E, Hiwasa-Tanase K, Fukuda N, Mizoguchi T, Yamazaki Y, Aoki K, Ezura H. TOMATOMA: a novel tomato mutant database distributing micro-tom mutant collections. Plant Cell Physiol. 2011;52:283–96. Just D, Garcia V, Fernandez L, Bres C, Mauxion J, Petit J, Jorly J, Assali J, Bournonville C, Ferrand C, Baldet P, Lemaire-Chamley M, Mori K, Okabe Y, Ariizumi T, Asamizu E, Ezura H, Rothan C. Micro-tom mutants for functional analysis of target genes and discovery of new alleles in tomato. Plant Biotechnol. 2013;30:225–31. Petit J, Bres C, Just D, Garcia V, Marion D, Bakan B, Joubes J, Domergue F, Rothan C. Analyses of tomato fruit brightness mutants uncover strong cutin-deficient mutants among which a new allele of GDSL lipase. Plant Physiol. 2014;164:888–906. Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, Jorgenesen JE, Weigel D, Andersen US. SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Methods. 2009;6:550–1. Garcia V, Bres C, Just D, Fernandez L, Tai FW, Mauxion JP, Le Paslier MC, Bérard A, Brunel D, Aoki K, Alseekh S, Fernie AR, Fraser PD, Rothan C. Rapid identification of causal mutations in tomato EMS populations via mappingby-sequencing. Nat Protoc. 2016;11:2401–18 Springer PS. Gene traps: tools for plant development and genomics. Plant Cell. 2000;12:1007–20 Pérez-Martín F, Yuste-Lisbona F, Pineda B, Angarita-Díaz M, García-Sogo B, Antón T, Sánchez S, Giménez-Caminero E, Atarés A, Fernández-Lozano A, Ortíz-Atienza A, García-Alcázar M, Castañeda L, Fonseca R, Capel C, Goergen G, Sánchez J, Quispe J, Capel J, Angosto T, Moreno V, Lozano R. A collection of enhancer trap insertional mutants for functional genomics in tomato. Plant Biotechnol J. 2017;15:1439–52. García-Alcázar M, Giménez E, Pineda B, Capel C, García-Sogo B, Sánchez S, Yuste-Lisbona FJ, Angosto T, Capel J, Moreno V, Lozano R. Albino T-DNA tomato mutant reveals a key function of 1-deoxy-D-xylulose-5-phosphate synthase (DXS1) in plant development and survival. Sci Rep. 2017;7:45333. Brand A, Shirding N, Shleizer S, Ori N. Meristem maintenance and compound-leaf patterning utilize common genetic mechanisms in tomato. Planta. 2007;226:941–51 Busch BL, Schmitz G, Rossmann S, Piron F, Ding J, Bendahmane A, Theres K. Shoot branching and leaf dissection in tomato are regulated by homologous gene modules. Plant Cell. 2011;23:3595–609 David-Schwartz R, Koenig D, Sinha NR. LYRATE is a key regulator of leaflet initiation and lamina outgrowth in tomato. Plant Cell. 2009;21:3093–104. Simmons AT, Gurr GM. Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies. Agric Forest Entomol. 2005;7:265–76. Guo ZH, Weston PA, Snyder JC. Repellency to 2-spotted spider-mite, Tetranychus urticae Koch, as related to leaf surface-chemistry of Lycopersicon hirsutum accessions. J Chem Ecol. 1993;19:2965–79 Walters DS, Steffens JC. Branched-chain amino-acid-metabolism in the biosynthesis of Lycopersicon pennellii glucose esters. Plant Physiol. 1990;93: 1544–51. Fernández-Muñoz R, Domínguez E, Cuartero J. A novel source of resistence to the two-spotted spider mite in Lycopersicon pimpinellifolium (Jusl.) Mill.: its genetics as affected by interplot interference. Euphytica. 2000;111:169–73. Fernández-Muñoz R, Salinas M, Álvarez M, Cuartero J. Inheritance of resistance to two-spotted spider mite and glandular leaf trichomes in wild tomato Lycopersicon pimpinellifolium (Jusl.) Mill. J Amer Soc Hort Sci. 2003;128:188–95 Salinas M, Capel C, Alba JM, Mora B, Cuartero J, Fernández-Muñoz R, Lozano R, Capel J. Genetic mapping of two QTL from the wild tomato Solanum pimpinellifolium L. controlling resistance against two-spotted spider mite (Tetranychus urticae Koch). Theor Appl Genet. 2013;126:83–92. Rodríguez-López MJ, Garzo E, Bonani JP, Fereres A, Fernández-Muñoz R, Moriones E. Whitefly resistance traits derived from the wild tomato Solanum pimpinellifolium affect the preference and feeding behavior of Bemisia tabaci and reduce the spread of tomato yellow leaf curl virus. Phytopatology. 2011;101:1191–201. Jeon JS, Lee S, Jung KH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam J, An K, Han MJ, Sung RJ, Choi HS, Yu JH, Cho SY, Cha SS, Kim SI, An G. T-DNA insertional mutagenesis for functional genomics in rice. Plant J. 2000;22:561–70. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen HM, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003;301:653–7 Larkin PJ, Scowcroft WR. Somaclonal variation - a novel source of variability from cell cultures for plant improvement. Theor Appl Genet. 1981;60:197–214 Clouse SD. A history of brassinosteroid research from 1970 through 2005: thirty-five years of phytochemistry, physiology, genes, and mutants. J Plant Growth Regul. 2015;34:828–44. Clouse SD, Langford M, McMorris TC. A brassinosteroids insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 1996;111:671–8 Clouse SD. Brassinosteroids, The Arabidopsis Book; 2011. https://doi.org/10. 1199/tab.0151. Montoya T, Nomura T, Farrar K, Kaneta T, Yokota T, Bishop GJ. Cloning the tomato Curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptid hormone signaling. Plant Cell. 2002;14:3163–76. Bishop G, Harrison K, Jones J. The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family. Plant Cell. 1996;8:959–69 Shimada Y, Fujioka S, Miyauchi N, Kushiro M, Takatsuto S, Nomura T, Yokota T, Kamiya Y, Bishop GJ, Yoshida S. Brassinosteroid-6-oxidases from Arabidopsis and tomato catalyze multiple C-6 oxidations in brassinosteroid biosynthesis. Plant Physiol. 2001;126:770–9. Koka CV, Cerny RE, Gardner RG, Noguchi T, Fujioka S, Takatsuto S, Yoshida S, Clouse SD. A putative role for the tomato genes DUMPY and CURL-3 in brassinosteroid biosynthesis and response. Plant Physiol. 2000;122:85–98. Yu MH. The dwarf curly leaf tomato mutant. J Hered. 1982;73:470–2 Atarés A, Moyano E, Morales B, Schleicher P, García-Abellán JO, Antón MT, GarcíaSogo B, Pérez-Martín F, Lorano R, Flores FB, Moreno V, Bolarín MC, Pineda B. An insertional mutagenesis programme with an enhancer trap for the identification and tagging of genes involved in abiotic stress tolerance in the tomato wildrelated species Solanum pennellii. Plant Cell Rep. 2011;30:1865–79 Yifhar T, Pekker I, Peled D, Friedlander G, Pistunov A, Sabban M, Wachsman G, Alvarez JP, Amsellem Z, Eshed Y. Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell. 2012;24:3575–89 Rubio-Somoza I, Cuperus JT, Weige D, Carrington JC. Regulation and functional specialization of small RNA-target nodes during plant development. Curr Opin Plant Biol. 2009;12:622–7 Alvarado V, Scholthof HB. Plant responses against invasive nucleic acids: RNA silencing and its suppression by plant viral pathogens. Semin Cell Dev Biol. 2009;20:1032–40. Mach J. Why wiry? Tomato mutants reveal connections among small RNAs, auxin response factors, virus infection, and leaf morphology. Plant Cell. 2012;24:3486. Lin D, Xiang Y, Xian Z, Li Z. Ectopic expression of SlAGO7 alters leaf pattern and inflorescence architecture and increases fruit yield in tomato. Physiol Plant. 2016;157:490–506. Nath U, Crawford BCW, Carpenter R, Coen E. Genetic control of surface curvature. Science. 2003;299:1404–7 Crawford BCW, Nath U, Carpenter R, Coen ES. CINCINNATA controls both cell differentiation and growth in petal lobes and leaves of Antirrhinum. Plant Physiol. 2004;135:244–53. Gupta M, Aggarwal P, Nath U. CINCINNATA in Antirrhinum majus directly modulates genes involved in cytokinin and auxin signaling. New Phytol. 2014;204:901–12 Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K. The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. PNAS. 1999;96:290–5. Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T. The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Development. 2000;127: 4443–53. Thitamadee S, Tuchihara K, Hashimoto T. Microtubule basis for left-handed helical growth in Arabidopsis. Nature. 2002;417:193–6 Buschmann H, Fabri CO, Hauptmann M, Hutzler P, Laux T, Lloyd CW, Schaffner AR. Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr Biol. 2004;14:1515–21. Buschmann H, Hauptmann M, Niessing D, Lloyd CW, Schaffner AR. Growth of the Arabidopsis mutant tortifolia2 does not depend on cell division patterns but involves handed twisting of isolated cells. Plant Cell. 2009;21:2090–106. Smith LG, Hake S, Sylvester AW. The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development. 1996;122:481–9. Martinez P, Luoc A, Sylvesterc A, Rasmussen CG. Proper division plane orientation and mitotic progression together allow normal growth of maize. PNAS. 2017;114:2759–64 Pineda B, Giménez-Caminero E, García-Sogo B, Antón MT, Atarés A, Capel J, Lozano R, Angosto T, Moreno V. Genetic and physiological characterization of the Arlequin insertional mutant reveals a key regulator of reproductive development in tomato. Plant Cell Physiol. 2010;51:435–47. Giménez-Caminero E, Pineda B, Capel J, Antón MT, Atarés A, Pérez-Martín F, García-Sogo B, Angosto T, Moreno V, Lozano R. Functional analysis of the Arlequin mutant corroborates the essential role of the ARLEQUIN/TAGL1 gene during reproductive development of tomato. Plos One. 2010;5(12):e1442. https://doi.org/10.1371/journal.pone.0014427. Mao L, Begum D, Chuang H, Budiman MA, Szymkowiak EJ, Irish EE, Wing RA. JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development. Nature. 2000;406:910–3. Gomez MV, Périlleux C, Morin H, Huerga-Fernandez S, Latrasse D, Benhamed M, Bendahmane A. Natural and induced loss of function mutations in SlMBP21 MADS-box gene led to jointless-2 phenotype in tomato. Sci Rep. 2017;7:4402 Liu DM, Wang D, Quin ZR, Zhang DD, Yin LJ, Wu L, Colasanti J, Li AL, Mao L. The SEPALLATA MADS-box protein SLMBP21 forms protein complexes with JOINTLESS and MACROCALYX as a transcription activator for development of the tomato flower abscission zone. Plant J. 2014;77:284–96. Kimura S, Koenig D, Kang J, Yoong FI, Sinha N. Natural variation in leaf morphology results from mutation of a novel KNOX gene. Curr Biol. 2008;18:672–7. Ma C, Meir S, Xiao L, Tong J, Liu Q, Reid MS, Jiang C-Z. A KNOTTED1-LIKE HOMEOBOX protein regulates abscission in tomato by modulating the auxin pathway. Plant Physiol. 2015;167:844–53. Thurber CS, Hepler PK, Caicedo AN. Timing is everything: early degradation of abscission layer is associated with increased seed shattering in U.S. weedy rice. BMC Plant Biol. 2011;11:14. Stenvik GE, Butenko MA, Urbanowicz BR, Rose JK, Aalen RB. Overexpression of INFLORESCENCE DEFICIENT IN ABSCISSION activates cell separation in vestigial abscission zone in Arabidopsis. Plant Cell. 2006;18:1467–76 Nakano T, Ito Y. Molecular mechanisms controlling plant organ abscission. Plant Biotech. 2013;30:209–16. Nakano T, Kimbara J, Fujisawa M, Kitagawa M, Ihashi N, Maeda H, Kasumi T, Ito Y. MACROCALYX and JOINTLESS interact in the transcriptional regulation of tomato fruit abscission zone development. Plant Physiol. 2012;158:439–50. Nakano T, Fujisawa M, Shima Y, Ito Y. Expression profiling of tomato preabscission pedicels provides insights into abscission zone properties including competence to respond to abscission signals. BMC Plant Biol. 2013;13:40. 74. Butenko MA, Simon R. Beyond the meristems: similarities in the CLAVATA3 and INFLORESCENCE DEFICIENT IN ABSCISSION peptide mediated signalling pathways. J Exp Bot. 2015;66:5195–203. Pérez-Martín F, Yuste-Lisbona F, Pineda B, García-Sogo B, del Olmo I, Alché JD, Egea I, Flores F, Pineiro M, Jarillo J, Angosto T, Capel J, Moreno V, Lozano R. Developmental role of the tomato mediator complex subunit MED18 in pollen ontogeny. Plant J. 2018;96:300–15. Kornberg RD. Mediator and the mechanism of transcriptional activation. Trends Biochem Sci. 2005;30:235–9. Bourbon HM. Comparative genomics supports a deep evolutionary origin for the large four-module transcriptional mediator complex. Nucleic Acids Res. 2008;36:3993–4008 Wang Y, Hu Z, Zhang J, Yu X, Guo JE, Liang H, Liao C, Chen G. Silencing SlMED18, tomato mediator subunit 18 gene, restricts internode elongation and leaf expansion. Sci Rep. 2018;8:3285. Burger C, Rondet S, Benveniste P, Schaller H. Virus-induced silencing of sterol biosynthetic genes: identification of a Nicotiana tabacum L. obtusifoliol-14alpha-demethylase (CYP51) by genetic manipulation of the sterol biosynthetic pathway in Nicotiana benthamiana L. J Exp Bot. 2003;54:1675–83. Duperon R, Thiersault M, Duperon P. High level of glycosylated sterols in species of Solanum and sterol changes during the development of the tomato. Phytochemistry. 1984;23:743–6. Steel CC, Drysdale RB. Electrolyte leakage from plant and fungal tissues and disruption of liposome membranes by α-tomatine. Phytochemistry. 1988;27:1025–30 Keukens EAJ, de Vrije T, van den Boom C, de Waard P, Plasman HH, Thiel F, Chupin V, Jongen WMF, de Kruijff B. Molecular basis of glycoalkaloid induced membrane disruption. BBA-Biomembranes. 1995;1240:216–28 Blankemeyer JT, White JB, Stringer BK, Friedman M. Effect of α-tomatine and tomatidine on membrane potential of frog embryos and active transport of ions in frog skin. Food Chem Toxicol. 1997;35:639–46. Ellul P, Ríos G, Atarés A, Roig LA, Serrano R, Moreno V. The expression of the Saccharomyces cerevisiae HAL1 gene increases salt tolerance in transgenic watermelon [Citrullus lanatus (Thunb.) Matsun. & Nakai.]. Theor Appl Genet. 2003;107:462–9. Campisi L, Yang Y, Yi Y, Heiling E, Herman B, Cassista AJ, Allen DW. Generation of enhancer trap lines in Arabidopsis and characterization of expression patterns in the inflorescence. Plant J. 1999;17:699–707. Murashige T, Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plan. 1962;15:473–97 Moreno V, Zubeldia L, Roig LA. A method for obtaining callus-cultures from mesophyll protoplasts of melon (Cucumis melo L.). Plant Sci Lett. 1984;34:195–201 Winer J, Jung CK, Shackel I, Williams PM. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem. 1999;15:41–9. |
| dc.rights.license.none.fl_str_mv |
Atribución |
| dc.rights.accessrights.none.fl_str_mv |
info:eu-repo/semantics/openAccess |
| dc.rights.coar.none.fl_str_mv |
http://purl.org/coar/access_right/c_abf2 |
| rights_invalid_str_mv |
Atribución http://purl.org/coar/access_right/c_abf2 |
| eu_rights_str_mv |
openAccess |
| dc.format.extent.spa.fl_str_mv |
1-24 |
| dc.coverage.temporal.spa.fl_str_mv |
19/141 |
| dc.publisher.spa.fl_str_mv |
Akila Sridhar, BioMed Central, UK Universidad Cooperativa de Colombia, Facultad de Ciencias de la Salud, Odontología, Villavicencio |
| dc.publisher.program.spa.fl_str_mv |
Odontología |
| dc.publisher.place.spa.fl_str_mv |
Villavicencio |
| institution |
Universidad Cooperativa de Colombia |
| bitstream.url.fl_str_mv |
https://repository.ucc.edu.co/bitstreams/a6100c51-1e71-44d7-8403-cf810906e4bb/download |
| bitstream.checksum.fl_str_mv |
3bce4f7ab09dfc588f126e1e36e98a45 |
| bitstream.checksumAlgorithm.fl_str_mv |
MD5 |
| repository.name.fl_str_mv |
Repositorio Institucional Universidad Cooperativa de Colombia |
| repository.mail.fl_str_mv |
bdigital@metabiblioteca.com |
| _version_ |
1814246981517705216 |
| spelling |
Jáquez Gutiérrez, MarybelAtarés, AlejandroPineda, BenitoAngarita Díaz, María del PilarRibelles, CarlosGarcía Sogo, BegoñaSánchez López, JorgeCapel, CarmenYuste Lisbona, FernandoLozano, RafaelMoreno, Vicente19/1412020-04-15T20:21:40Z2020-04-15T20:21:40Z2019-04-15https://doi.org/10.1186/s12870-019-1735-9https://hdl.handle.net/20.500.12494/17418Jáquez Gutiérrez, M., Atarés, A., Pineda, B., Angarita, P., Ribelles, C., García Sogo, B. ... Moreno, V. (2019). Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits. BMC Plant Biol 19, 141. https://doi.org/10.1186/s12870-019-1735-9Background: Tomato mutants altered in leaf morphology are usually identified in the greenhouse, which demands considerable time and space and can only be performed in adequate periods. For a faster but equally reliable scrutiny method we addressed the screening in vitro of 971 T-DNA lines. Leaf development was evaluated in vitro in seedlings and shoot-derived axenic plants. New mutants were characterized in the greenhouse to establish the relationship between in vitro and in vivo leaf morphology, and to shed light on possible links between leaf development and agronomic traits, a promising field in which much remains to be discovered. Results: Following the screening in vitro of tomato T-DNA lines, putative mutants altered in leaf morphology were evaluated in the greenhouse. The comparison of results in both conditions indicated a general phenotypic correspondence, showing that in vitro culture is a reliable system for finding mutants altered in leaf development. Apart from providing homogeneous conditions, the main advantage of screening in vitro lies in the enormous time and space saving. Studies on the association between phenotype and nptII gene expression showed co-segregation in two lines (P > 99%). The use of an enhancer trap also allowed identifying gain-of-function mutants through reporter expression analysis. These studies suggested that genes altered in three other mutants were T-DNA tagged. New mutants putatively altered in brassinosteroid synthesis or perception, mutations determining multiple pleiotropic effects, lines affected in organ curvature, and the first tomato mutant with helical growth were discovered. Results also revealed new possible links between leaf development and agronomic traits, such as axillary branching, flower abscission, fruit development and fruit cracking. Furthermore, we found that the gene tagged in mutant 2635-MM encodes a Sterol 3-beta-glucosyltransferase. Expression analysis suggested that abnormal leaf development might be due to the lack-off-function of this gene. Conclusion: In vitro culture is a quick, efficient and reliable tool for identifying tomato mutants altered in leaf morphology. The characterization of new mutants in vivo revealed new links between leaf development and some agronomic traits. Moreover, the possible implication of a gene encoding a Sterol 3-beta-glucosyltransferase in tomato leaf development is reported.http://scienti.colciencias.gov.co:8081/cvlac/visualizador/generarCurriculoCv.do?cod_rh=0001561382https://orcid.org/0000-0002-5435-3456maria.angaritad@campusucc.edu.co1-24Akila Sridhar, BioMed Central, UKUniversidad Cooperativa de Colombia, Facultad de Ciencias de la Salud, Odontología, VillavicencioOdontologíaVillavicenciohttps://link.springer.com/article/10.1186/s12870-019-1735-9BMC Plant BiologyLi N, Jia J, Xia C, Liu X, Kong X. Characterization and mapping of novel chlorophyll deficient mutant genes in durum wheat. Breed Sci. 2013;63:169–75Aluru MR, Yu F, Fu AG, Rodermel S. Arabidopsis variegation mutants: new insights into chloroplast biogenesis. J Exp Bot. 2006;57:1871–81.Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E. The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell. 1996;84:735–44Efroni I, Eshed Y, Lifschitz E. Morphogenesis of simple and compound leaves: a critical review. Plant Cell. 2010;22:1019–32.Gonzalez N, Vanhaeren H, Inze D. Leaf size control: complex coordination of cell division expansion. Trends Plant Sci. 2012;17:332–40.Tsukaya H. Leaf Development, The Arabidopsis Book; 2013. https://doi.org/ 10.1199/tab.0163Kessler S, Kim M, Pham T, Weber N, Sinha N. Mutations altering leaf morphology in tomato. Int J Plant Sci. 2001;162:475–92.Sarlikioti V, de Visser PHB, Buck-Sorlin GH, Marcelis LFM. How plant architecture affects light absorption and photosynthesis in tomato: towards an ideotype for plant architecture using a functional–structural plant model. Ann Bot. 2011;108:1065–73Rothan C, Bres C, Garcia V, Just D. Tomato resources for functional genomics. In: Causse M, Giovannoni J, Bouzayen M, Zouine M, editors. The tomato genome. Compendium of plant genomes. Berlin: Springer; 2016. p. 75–94.Menda N, Semel Y, Peled D, Eshed Y, Zamir D. In silico screening of a saturated mutation library of tomato. Plant J. 2004;38:861–72Meissner R, Jacobson Y, Melamed S, Levyatuv S, Shalev G, Ashri A, Elkind Y, Levy A. A new model system for tomato genetics. Plant J. 1997;12:1465–72.Dan Y, Fei Z, Rothan C. Micro-tom - a new model plant for genomics. Genes Genomes Genomics. 2007;1:167–79.Matsukura C, Yamaguchi I, Inamura M, Ban Y, Kobayashi Y, Yin YG, Saito T, Kuwata C, Imanishi S, Nishimura S. Generation of gamma irradiationinduced mutant lines of the miniature tomato (Solanum lycopersicum L.) cultivar ‘Micro-Tom’. Plant Biotechnol. 2007;24:39–44Watanabe S, Mizoguchi T, Aoki K, Kubo Y, Mori H, Imanishi S, Yamazaki Y, Shibata D, Ezura H. Ethylmethanesulfonate (EMS) mutagenesis of Solanum lycopercisum cv. Micro-tom for large-scale mutant screens. Plant Biotech. 2007;24:33–8Minoia S, Petrozza A, D’Onofrio O, Piron F, Mosca G, Sozio G, Cellini F, Bendahmane A, Carriero F. A new mutant genetic resource for tomato crop improvement by TILLING technology. BMC Res Notes. 2010;3:69.Okabe Y, Asamizu E, Saito T, Matsukura C, Ariizumi T, Brès C, Rothan C, Mizoguchi T, Ezura H. Tomato TILLING technology: development of a reverse genetics tool for the efficient isolation of mutants from micro-tom mutant libraries. Plant Cell Physiol. 2011;52:1994–2005.Saito T, Ariizumi T, Okabe Y, Asamizu E, Hiwasa-Tanase K, Fukuda N, Mizoguchi T, Yamazaki Y, Aoki K, Ezura H. TOMATOMA: a novel tomato mutant database distributing micro-tom mutant collections. Plant Cell Physiol. 2011;52:283–96.Just D, Garcia V, Fernandez L, Bres C, Mauxion J, Petit J, Jorly J, Assali J, Bournonville C, Ferrand C, Baldet P, Lemaire-Chamley M, Mori K, Okabe Y, Ariizumi T, Asamizu E, Ezura H, Rothan C. Micro-tom mutants for functional analysis of target genes and discovery of new alleles in tomato. Plant Biotechnol. 2013;30:225–31.Petit J, Bres C, Just D, Garcia V, Marion D, Bakan B, Joubes J, Domergue F, Rothan C. Analyses of tomato fruit brightness mutants uncover strong cutin-deficient mutants among which a new allele of GDSL lipase. Plant Physiol. 2014;164:888–906.Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, Jorgenesen JE, Weigel D, Andersen US. SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Methods. 2009;6:550–1.Garcia V, Bres C, Just D, Fernandez L, Tai FW, Mauxion JP, Le Paslier MC, Bérard A, Brunel D, Aoki K, Alseekh S, Fernie AR, Fraser PD, Rothan C. Rapid identification of causal mutations in tomato EMS populations via mappingby-sequencing. Nat Protoc. 2016;11:2401–18Springer PS. Gene traps: tools for plant development and genomics. Plant Cell. 2000;12:1007–20Pérez-Martín F, Yuste-Lisbona F, Pineda B, Angarita-Díaz M, García-Sogo B, Antón T, Sánchez S, Giménez-Caminero E, Atarés A, Fernández-Lozano A, Ortíz-Atienza A, García-Alcázar M, Castañeda L, Fonseca R, Capel C, Goergen G, Sánchez J, Quispe J, Capel J, Angosto T, Moreno V, Lozano R. A collection of enhancer trap insertional mutants for functional genomics in tomato. Plant Biotechnol J. 2017;15:1439–52.García-Alcázar M, Giménez E, Pineda B, Capel C, García-Sogo B, Sánchez S, Yuste-Lisbona FJ, Angosto T, Capel J, Moreno V, Lozano R. Albino T-DNA tomato mutant reveals a key function of 1-deoxy-D-xylulose-5-phosphate synthase (DXS1) in plant development and survival. Sci Rep. 2017;7:45333.Brand A, Shirding N, Shleizer S, Ori N. Meristem maintenance and compound-leaf patterning utilize common genetic mechanisms in tomato. Planta. 2007;226:941–51Busch BL, Schmitz G, Rossmann S, Piron F, Ding J, Bendahmane A, Theres K. Shoot branching and leaf dissection in tomato are regulated by homologous gene modules. Plant Cell. 2011;23:3595–609David-Schwartz R, Koenig D, Sinha NR. LYRATE is a key regulator of leaflet initiation and lamina outgrowth in tomato. Plant Cell. 2009;21:3093–104.Simmons AT, Gurr GM. Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies. Agric Forest Entomol. 2005;7:265–76.Guo ZH, Weston PA, Snyder JC. Repellency to 2-spotted spider-mite, Tetranychus urticae Koch, as related to leaf surface-chemistry of Lycopersicon hirsutum accessions. J Chem Ecol. 1993;19:2965–79Walters DS, Steffens JC. Branched-chain amino-acid-metabolism in the biosynthesis of Lycopersicon pennellii glucose esters. Plant Physiol. 1990;93: 1544–51.Fernández-Muñoz R, Domínguez E, Cuartero J. A novel source of resistence to the two-spotted spider mite in Lycopersicon pimpinellifolium (Jusl.) Mill.: its genetics as affected by interplot interference. Euphytica. 2000;111:169–73.Fernández-Muñoz R, Salinas M, Álvarez M, Cuartero J. Inheritance of resistance to two-spotted spider mite and glandular leaf trichomes in wild tomato Lycopersicon pimpinellifolium (Jusl.) Mill. J Amer Soc Hort Sci. 2003;128:188–95Salinas M, Capel C, Alba JM, Mora B, Cuartero J, Fernández-Muñoz R, Lozano R, Capel J. Genetic mapping of two QTL from the wild tomato Solanum pimpinellifolium L. controlling resistance against two-spotted spider mite (Tetranychus urticae Koch). Theor Appl Genet. 2013;126:83–92.Rodríguez-López MJ, Garzo E, Bonani JP, Fereres A, Fernández-Muñoz R, Moriones E. Whitefly resistance traits derived from the wild tomato Solanum pimpinellifolium affect the preference and feeding behavior of Bemisia tabaci and reduce the spread of tomato yellow leaf curl virus. Phytopatology. 2011;101:1191–201.Jeon JS, Lee S, Jung KH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam J, An K, Han MJ, Sung RJ, Choi HS, Yu JH, Cho SY, Cha SS, Kim SI, An G. T-DNA insertional mutagenesis for functional genomics in rice. Plant J. 2000;22:561–70.Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen HM, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003;301:653–7Larkin PJ, Scowcroft WR. Somaclonal variation - a novel source of variability from cell cultures for plant improvement. Theor Appl Genet. 1981;60:197–214Clouse SD. A history of brassinosteroid research from 1970 through 2005: thirty-five years of phytochemistry, physiology, genes, and mutants. J Plant Growth Regul. 2015;34:828–44.Clouse SD, Langford M, McMorris TC. A brassinosteroids insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 1996;111:671–8Clouse SD. Brassinosteroids, The Arabidopsis Book; 2011. https://doi.org/10. 1199/tab.0151.Montoya T, Nomura T, Farrar K, Kaneta T, Yokota T, Bishop GJ. Cloning the tomato Curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptid hormone signaling. Plant Cell. 2002;14:3163–76.Bishop G, Harrison K, Jones J. The tomato Dwarf gene isolated by heterologous transposon tagging encodes the first member of a new cytochrome P450 family. Plant Cell. 1996;8:959–69Shimada Y, Fujioka S, Miyauchi N, Kushiro M, Takatsuto S, Nomura T, Yokota T, Kamiya Y, Bishop GJ, Yoshida S. Brassinosteroid-6-oxidases from Arabidopsis and tomato catalyze multiple C-6 oxidations in brassinosteroid biosynthesis. Plant Physiol. 2001;126:770–9.Koka CV, Cerny RE, Gardner RG, Noguchi T, Fujioka S, Takatsuto S, Yoshida S, Clouse SD. A putative role for the tomato genes DUMPY and CURL-3 in brassinosteroid biosynthesis and response. Plant Physiol. 2000;122:85–98.Yu MH. The dwarf curly leaf tomato mutant. J Hered. 1982;73:470–2Atarés A, Moyano E, Morales B, Schleicher P, García-Abellán JO, Antón MT, GarcíaSogo B, Pérez-Martín F, Lorano R, Flores FB, Moreno V, Bolarín MC, Pineda B. An insertional mutagenesis programme with an enhancer trap for the identification and tagging of genes involved in abiotic stress tolerance in the tomato wildrelated species Solanum pennellii. Plant Cell Rep. 2011;30:1865–79Yifhar T, Pekker I, Peled D, Friedlander G, Pistunov A, Sabban M, Wachsman G, Alvarez JP, Amsellem Z, Eshed Y. Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell. 2012;24:3575–89Rubio-Somoza I, Cuperus JT, Weige D, Carrington JC. Regulation and functional specialization of small RNA-target nodes during plant development. Curr Opin Plant Biol. 2009;12:622–7Alvarado V, Scholthof HB. Plant responses against invasive nucleic acids: RNA silencing and its suppression by plant viral pathogens. Semin Cell Dev Biol. 2009;20:1032–40.Mach J. Why wiry? Tomato mutants reveal connections among small RNAs, auxin response factors, virus infection, and leaf morphology. Plant Cell. 2012;24:3486.Lin D, Xiang Y, Xian Z, Li Z. Ectopic expression of SlAGO7 alters leaf pattern and inflorescence architecture and increases fruit yield in tomato. Physiol Plant. 2016;157:490–506.Nath U, Crawford BCW, Carpenter R, Coen E. Genetic control of surface curvature. Science. 2003;299:1404–7Crawford BCW, Nath U, Carpenter R, Coen ES. CINCINNATA controls both cell differentiation and growth in petal lobes and leaves of Antirrhinum. Plant Physiol. 2004;135:244–53.Gupta M, Aggarwal P, Nath U. CINCINNATA in Antirrhinum majus directly modulates genes involved in cytokinin and auxin signaling. New Phytol. 2014;204:901–12Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K. The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. PNAS. 1999;96:290–5.Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T. The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Development. 2000;127: 4443–53.Thitamadee S, Tuchihara K, Hashimoto T. Microtubule basis for left-handed helical growth in Arabidopsis. Nature. 2002;417:193–6Buschmann H, Fabri CO, Hauptmann M, Hutzler P, Laux T, Lloyd CW, Schaffner AR. Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr Biol. 2004;14:1515–21.Buschmann H, Hauptmann M, Niessing D, Lloyd CW, Schaffner AR. Growth of the Arabidopsis mutant tortifolia2 does not depend on cell division patterns but involves handed twisting of isolated cells. Plant Cell. 2009;21:2090–106.Smith LG, Hake S, Sylvester AW. The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development. 1996;122:481–9.Martinez P, Luoc A, Sylvesterc A, Rasmussen CG. Proper division plane orientation and mitotic progression together allow normal growth of maize. PNAS. 2017;114:2759–64Pineda B, Giménez-Caminero E, García-Sogo B, Antón MT, Atarés A, Capel J, Lozano R, Angosto T, Moreno V. Genetic and physiological characterization of the Arlequin insertional mutant reveals a key regulator of reproductive development in tomato. Plant Cell Physiol. 2010;51:435–47.Giménez-Caminero E, Pineda B, Capel J, Antón MT, Atarés A, Pérez-Martín F, García-Sogo B, Angosto T, Moreno V, Lozano R. Functional analysis of the Arlequin mutant corroborates the essential role of the ARLEQUIN/TAGL1 gene during reproductive development of tomato. Plos One. 2010;5(12):e1442. https://doi.org/10.1371/journal.pone.0014427.Mao L, Begum D, Chuang H, Budiman MA, Szymkowiak EJ, Irish EE, Wing RA. JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development. Nature. 2000;406:910–3.Gomez MV, Périlleux C, Morin H, Huerga-Fernandez S, Latrasse D, Benhamed M, Bendahmane A. Natural and induced loss of function mutations in SlMBP21 MADS-box gene led to jointless-2 phenotype in tomato. Sci Rep. 2017;7:4402Liu DM, Wang D, Quin ZR, Zhang DD, Yin LJ, Wu L, Colasanti J, Li AL, Mao L. The SEPALLATA MADS-box protein SLMBP21 forms protein complexes with JOINTLESS and MACROCALYX as a transcription activator for development of the tomato flower abscission zone. Plant J. 2014;77:284–96.Kimura S, Koenig D, Kang J, Yoong FI, Sinha N. Natural variation in leaf morphology results from mutation of a novel KNOX gene. Curr Biol. 2008;18:672–7.Ma C, Meir S, Xiao L, Tong J, Liu Q, Reid MS, Jiang C-Z. A KNOTTED1-LIKE HOMEOBOX protein regulates abscission in tomato by modulating the auxin pathway. Plant Physiol. 2015;167:844–53.Thurber CS, Hepler PK, Caicedo AN. Timing is everything: early degradation of abscission layer is associated with increased seed shattering in U.S. weedy rice. BMC Plant Biol. 2011;11:14.Stenvik GE, Butenko MA, Urbanowicz BR, Rose JK, Aalen RB. Overexpression of INFLORESCENCE DEFICIENT IN ABSCISSION activates cell separation in vestigial abscission zone in Arabidopsis. Plant Cell. 2006;18:1467–76Nakano T, Ito Y. Molecular mechanisms controlling plant organ abscission. Plant Biotech. 2013;30:209–16.Nakano T, Kimbara J, Fujisawa M, Kitagawa M, Ihashi N, Maeda H, Kasumi T, Ito Y. MACROCALYX and JOINTLESS interact in the transcriptional regulation of tomato fruit abscission zone development. Plant Physiol. 2012;158:439–50.Nakano T, Fujisawa M, Shima Y, Ito Y. Expression profiling of tomato preabscission pedicels provides insights into abscission zone properties including competence to respond to abscission signals. BMC Plant Biol. 2013;13:40. 74.Butenko MA, Simon R. Beyond the meristems: similarities in the CLAVATA3 and INFLORESCENCE DEFICIENT IN ABSCISSION peptide mediated signalling pathways. J Exp Bot. 2015;66:5195–203.Pérez-Martín F, Yuste-Lisbona F, Pineda B, García-Sogo B, del Olmo I, Alché JD, Egea I, Flores F, Pineiro M, Jarillo J, Angosto T, Capel J, Moreno V, Lozano R. Developmental role of the tomato mediator complex subunit MED18 in pollen ontogeny. Plant J. 2018;96:300–15.Kornberg RD. Mediator and the mechanism of transcriptional activation. Trends Biochem Sci. 2005;30:235–9.Bourbon HM. Comparative genomics supports a deep evolutionary origin for the large four-module transcriptional mediator complex. Nucleic Acids Res. 2008;36:3993–4008Wang Y, Hu Z, Zhang J, Yu X, Guo JE, Liang H, Liao C, Chen G. Silencing SlMED18, tomato mediator subunit 18 gene, restricts internode elongation and leaf expansion. Sci Rep. 2018;8:3285.Burger C, Rondet S, Benveniste P, Schaller H. Virus-induced silencing of sterol biosynthetic genes: identification of a Nicotiana tabacum L. obtusifoliol-14alpha-demethylase (CYP51) by genetic manipulation of the sterol biosynthetic pathway in Nicotiana benthamiana L. J Exp Bot. 2003;54:1675–83.Duperon R, Thiersault M, Duperon P. High level of glycosylated sterols in species of Solanum and sterol changes during the development of the tomato. Phytochemistry. 1984;23:743–6.Steel CC, Drysdale RB. Electrolyte leakage from plant and fungal tissues and disruption of liposome membranes by α-tomatine. Phytochemistry. 1988;27:1025–30Keukens EAJ, de Vrije T, van den Boom C, de Waard P, Plasman HH, Thiel F, Chupin V, Jongen WMF, de Kruijff B. Molecular basis of glycoalkaloid induced membrane disruption. BBA-Biomembranes. 1995;1240:216–28Blankemeyer JT, White JB, Stringer BK, Friedman M. Effect of α-tomatine and tomatidine on membrane potential of frog embryos and active transport of ions in frog skin. Food Chem Toxicol. 1997;35:639–46.Ellul P, Ríos G, Atarés A, Roig LA, Serrano R, Moreno V. The expression of the Saccharomyces cerevisiae HAL1 gene increases salt tolerance in transgenic watermelon [Citrullus lanatus (Thunb.) Matsun. & Nakai.]. Theor Appl Genet. 2003;107:462–9.Campisi L, Yang Y, Yi Y, Heiling E, Herman B, Cassista AJ, Allen DW. Generation of enhancer trap lines in Arabidopsis and characterization of expression patterns in the inflorescence. Plant J. 1999;17:699–707.Murashige T, Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plan. 1962;15:473–97Moreno V, Zubeldia L, Roig LA. A method for obtaining callus-cultures from mesophyll protoplasts of melon (Cucumis melo L.). Plant Sci Lett. 1984;34:195–201Winer J, Jung CK, Shackel I, Williams PM. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem. 1999;15:41–9.TomatoT-DNA linesScreening in vitroMutantsLeaf developmentOrgan curvaturePhenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traitsArtículohttp://purl.org/coar/resource_type/c_6501http://purl.org/coar/resource_type/c_2df8fbb1http://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionAtribucióninfo:eu-repo/semantics/openAccesshttp://purl.org/coar/access_right/c_abf2PublicationLICENSElicense.txtlicense.txttext/plain; charset=utf-84334https://repository.ucc.edu.co/bitstreams/a6100c51-1e71-44d7-8403-cf810906e4bb/download3bce4f7ab09dfc588f126e1e36e98a45MD5220.500.12494/17418oai:repository.ucc.edu.co:20.500.12494/174182024-08-10 22:41:16.345metadata.onlyhttps://repository.ucc.edu.coRepositorio Institucional Universidad Cooperativa de Colombiabdigital@metabiblioteca.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 |