title: Transcriptomes of Eight Arabidopsis thaliana Accessions Reveal Core Conserved, Genotype- and Organ-Specific Responses to Flooding Stress.
abstract: Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity. These events often submerge plant aerial organs and roots, limiting growth and survival due to a severe reduction in light reactions and gas exchange necessary for photosynthesis and respiration, respectively. To distinguish molecular responses to the compound stress imposed by submergence, we investigated transcriptomic adjustments to darkness in air and under submerged conditions using eight Arabidopsis (Arabidopsis thaliana) accessions differing significantly in sensitivity to submergence. Evaluation of root and rosette transcriptomes revealed an early transcriptional and posttranscriptional response signature that was conserved primarily across genotypes, although flooding susceptibility-associated and genotype-specific responses also were uncovered. Posttranscriptional regulation encompassed darkness- and submergence-induced alternative splicing of transcripts from pathways involved in the alternative mobilization of energy reserves. The organ-specific transcriptome adjustments reflected the distinct physiological status of roots and shoots. Root-specific transcriptome changes included marked up-regulation of chloroplast-encoded photosynthesis and redox-related genes, whereas those of the rosette were related to the regulation of development and growth processes. We identified a novel set of tolerance genes, recognized mainly by quantitative differences. These included a transcriptome signature of more pronounced gluconeogenesis in tolerant accessions, a response that included stress-induced alternative splicing. This study provides organ-specific molecular resolution of genetic variation in submergence responses involving interactions between darkness and low-oxygen constraints of flooding stress and demonstrates that early transcriptome plasticity, including alternative splicing, is associated with the ability to cope with a compound environmental stress.
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Hans
authors.initials: H
authors.lastname: van Veen
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Divya
authors.initials: D
authors.lastname: Vashisht
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Melis
authors.initials: M
authors.lastname: Akman
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Thomas
authors.initials: T
authors.lastname: Girke
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Angelika
authors.initials: A
authors.lastname: Mustroph
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Emilie
authors.initials: E
authors.lastname: Reinen
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Sjon
authors.identifier: 0000-0002-6709-6436
authors.initials: S
authors.lastname: Hartman
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Maarten
authors.initials: M
authors.lastname: Kooiker
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Peter
authors.initials: P
authors.lastname: van Tienderen
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: M Eric
authors.identifier: 0000-0001-6777-6565
authors.initials: ME
authors.lastname: Schranz
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Julia
authors.identifier: 0000-0002-8568-7125
authors.initials: J
authors.lastname: Bailey-Serres
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.).
authors.forename: Laurentius A C J
authors.initials: LA
authors.lastname: Voesenek
authors.affiliation: Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 CH Utrecht, The Netherlands (H.v.V., D.V., E.R., S.H., M.K., J.B.-S., L.A.C.J.V., R.S.);Institute of Life Sciences, Scuola Superiore Sant'Anna, 56127 Pisa, Italy (H.v.V.);Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands (M.A., P.v.T.);Center for Plant Cell Biology, Botany, and Plant Sciences, University of California, Riverside, California 92521 (T.G., J.B.-S.);Department of Plant Physiology, Bayreuth University, 95447 Bayreuth, Germany (A.M.); andBiosystematics Group, Wageningen University, 6708 PB Wageningen, The Netherlands (M.E.S.) r.sasidharan@uu.nl.
authors.forename: Rashmi
authors.identifier: 0000-0002-6940-0657
authors.initials: R
authors.lastname: Sasidharan
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics / Q000528:radiation effects; D017360:Arabidopsis / Q000145:classification / Q000235:genetics*; D003624:Darkness; D055868:Floods; D020869:Gene Expression Profiling / Q000379:methods*; D018506:Gene Expression Regulation, Plant / Q000235:genetics* / Q000528:radiation effects; D063990:Gene Ontology; D005838:Genotype; D009928:Organ Specificity / Q000235:genetics; D010788:Photosynthesis / Q000235:genetics; D018517:Plant Roots / Q000235:genetics; D018520:Plant Shoots / Q000235:genetics; D020133:Reverse Transcriptase Polymerase Chain Reaction; D015398:Signal Transduction / Q000235:genetics; D013045:Species Specificity; D013312:Stress, Physiological; D059467:Transcriptome; D014867:Water / Q000378:metabolism
chemical_list: D014867:Water