title: Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome.
abstract: Interfering with small RNA production is a common strategy of plant viruses. A unique class of small RNAs that require microRNA and short interfering (siRNA) biogenesis for their production is termed trans-acting short interfering RNAs (ta-siRNAs). Tomato (Solanum lycopersicum) wiry mutants represent a class of phenotype that mimics viral infection symptoms, including shoestring leaves that lack leaf blade expansion. Here, we show that four WIRY genes are involved in siRNA biogenesis, and in their corresponding mutants, levels of ta-siRNAs that regulate AUXIN RESPONSE FACTOR3 (ARF3) and ARF4 are reduced, while levels of their target ARFs are elevated. Reducing activity of both ARF3 and ARF4 can rescue the wiry leaf lamina, and increased activity of either can phenocopy wiry leaves. Thus, a failure to negatively regulate these ARFs underlies tomato shoestring leaves. Overexpression of these ARFs in Arabidopsis thaliana, tobacco (Nicotiana tabacum), and potato (Solanum tuberosum) failed to produce wiry leaves, suggesting that the dramatic response in tomato is exceptional. As negative regulation of orthologs of these ARFs by ta-siRNA is common to land plants, we propose that ta-siRNA levels serve as universal sensors for interference with small RNA biogenesis, and changes in their levels direct species-specific responses.
authors.affiliation: Department of Plant Sciences, Weizman Institute of Science, Rehovot 76100, Israel.
authors.forename: Tamar
authors.initials: T
authors.lastname: Yifhar
authors.forename: Irena
authors.initials: I
authors.lastname: Pekker
authors.forename: Dror
authors.initials: D
authors.lastname: Peled
authors.forename: Gilgi
authors.initials: G
authors.lastname: Friedlander
authors.forename: Anna
authors.initials: A
authors.lastname: Pistunov
authors.forename: Moti
authors.initials: M
authors.lastname: Sabban
authors.forename: Guy
authors.initials: G
authors.lastname: Wachsman
authors.forename: John Paul
authors.initials: JP
authors.lastname: Alvarez
authors.forename: Ziva
authors.initials: Z
authors.lastname: Amsellem
authors.forename: Yuval
authors.initials: Y
authors.lastname: Eshed
mesh_terms: D000483:Alleles; D017360:Arabidopsis / Q000033:anatomy & histology / Q000235:genetics; D001483:Base Sequence; D018506:Gene Expression Regulation, Plant / Q000235:genetics*; D056426:Genetic Loci; D007210:Indoleacetic Acids / Q000378:metabolism; D018551:Solanum lycopersicum / Q000033:anatomy & histology / Q000235:genetics* / Q000502:physiology; D008969:Molecular Sequence Data; D009154:Mutation; D010641:Phenotype; D010937:Plant Growth Regulators / Q000378:metabolism; D018515:Plant Leaves / Q000033:anatomy & histology / Q000235:genetics* / Q000502:physiology; D010940:Plant Proteins / Q000235:genetics*; D018749:RNA, Plant / Q000235:genetics; D034741:RNA, Small Interfering / Q000235:genetics*; D017422:Sequence Analysis, DNA; D011198:Solanum tuberosum / Q000033:anatomy & histology / Q000235:genetics; D013045:Species Specificity; D014026:Nicotiana / Q000033:anatomy & histology / Q000235:genetics
chemical_list: D007210:Indoleacetic Acids; D010937:Plant Growth Regulators; D010940:Plant Proteins; D018749:RNA, Plant; D034741:RNA, Small Interfering