title: HsfA2 Controls the Activity of Developmentally and Stress-Regulated Heat Stress Protection Mechanisms in Tomato Male Reproductive Tissues.
abstract: Male reproductive tissues are more sensitive to heat stress (HS) compared to vegetative tissues, but the basis of this phenomenon is poorly understood. Heat stress transcription factors (Hsfs) regulate the transcriptional changes required for protection from HS In tomato (Solanum lycopersicum), HsfA2 acts as coactivator of HsfA1a and is one of the major Hsfs accumulating in response to elevated temperatures. The contribution of HsfA2 in heat stress response (HSR) and thermotolerance was investigated in different tissues of transgenic tomato plants with suppressed HsfA2 levels (A2AS). Global transcriptome analysis and immunodetection of two major Hsps in vegetative and reproductive tissues showed that HsfA2 regulates subsets of HS-induced genes in a tissue-specific manner. Accumulation of HsfA2 by a moderate HS treatment enhances the capacity of seedlings to cope with a subsequent severe HS, suggesting an important role for HsfA2 in regulating acquired thermotolerance. In pollen, HsfA2 is an important coactivator of HsfA1a during HSR HsfA2 suppression reduces the viability and germination rate of pollen that received the stress during the stages of meiosis and microspore formation but had no effect on more advanced stages. In general, pollen meiocytes and microspores are characterized by increased susceptibility to HS due to their lower capacity to induce a strong HSR This sensitivity is partially mitigated by the developmentally regulated expression of HsfA2 and several HS-responsive genes mediated by HsfA1a under nonstress conditions. Thereby, HsfA2 is an important factor for the priming process that sustains pollen thermotolerance during microsporogenesis.
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.).
authors.forename: Sotirios
authors.identifier: 0000-0001-5311-7868
authors.initials: S
authors.lastname: Fragkostefanakis
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.).
authors.forename: Anida
authors.identifier: 0000-0001-6277-5141
authors.initials: A
authors.lastname: Mesihovic
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.).
authors.forename: Stefan
authors.initials: S
authors.lastname: Simm
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.).
authors.forename: Marine Josephine
authors.initials: MJ
authors.lastname: Paupière
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.).
authors.forename: Yangjie
authors.identifier: 0000-0002-0910-6384
authors.initials: Y
authors.lastname: Hu
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.).
authors.forename: Puneet
authors.identifier: 0000-0001-8220-8021
authors.initials: P
authors.lastname: Paul
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.).
authors.forename: Shravan Kumar
authors.identifier: 0000-0003-3899-0495
authors.initials: SK
authors.lastname: Mishra
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.).
authors.forename: Bettina
authors.identifier: 0000-0002-6956-8804
authors.initials: B
authors.lastname: Tschiersch
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.).
authors.forename: Klaus
authors.initials: K
authors.lastname: Theres
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.).
authors.forename: Arnaud
authors.initials: A
authors.lastname: Bovy
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.) schleiff@bio.uni-frankfurt.de scharf@bio.uni-frankfurt.de.
authors.forename: Enrico
authors.initials: E
authors.lastname: Schleiff
authors.affiliation: Department of Biosciences, Molecular Cell Biology of Plants, Goethe University, D-60438 Frankfurt am Main, Germany (S.F., A.M., S.S., Y.H., P.P., S.K.M., E.S., K.-D.S.);Cluster of Excellence Frankfurt, Goethe University, D-60438 Frankfurt am Main, Germany (S.S., E.S.);Plant Breeding, Wageningen University, Wageningen 6708PB, The Netherlands (M.J.P., A.B.);Leibniz Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany (B.T., K.-D.S.);Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany (K.T.); andBuchmann Institute for Molecular Life Sciences, Goethe University, D-60438 Frankfurt am Main, Germany (E.S.) schleiff@bio.uni-frankfurt.de scharf@bio.uni-frankfurt.de.
authors.forename: Klaus-Dieter
authors.initials: KD
authors.lastname: Scharf
mesh_terms: D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism*; D035264:Flowers / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D056130:Gametogenesis, Plant; D020869:Gene Expression Profiling; D018507:Gene Expression Regulation, Developmental; D018506:Gene Expression Regulation, Plant; D000076249:Heat Shock Transcription Factors; D006360:Heat-Shock Proteins / Q000235:genetics / Q000378:metabolism*; D018869:Heat-Shock Response; D006358:Hot Temperature; D018551:Solanum lycopersicum / Q000235:genetics / Q000254:growth & development / Q000502:physiology*; D009928:Organ Specificity; D018515:Plant Leaves / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D030821:Plants, Genetically Modified; D011058:Pollen / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D036226:Seedlings / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D000071436:Thermotolerance; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*
chemical_list: D004268:DNA-Binding Proteins; D000076249:Heat Shock Transcription Factors; D006360:Heat-Shock Proteins; D010940:Plant Proteins; D014157:Transcription Factors