Transcriptional and Post-transcriptional Mechanisms Limit Heading Date 1 (Hd1) Function to Adapt Rice to High Latitudes

Rice flowering is controlled by changes in the photoperiod that promote the transition to the reproductive phase as days become shorter. Natural genetic variation for flowering time has been largely documented and has been instrumental to define the genetics of the photoperiodic pathway, as well as...

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Published inPLoS genetics Vol. 13; no. 1; p. e1006530
Main Authors Goretti, Daniela, Martignago, Damiano, Landini, Martina, Brambilla, Vittoria, Gómez-Ariza, Jorge, Gnesutta, Nerina, Galbiati, Francesca, Collani, Silvio, Takagi, Hiroki, Terauchi, Ryohei, Mantovani, Roberto, Fornara, Fabio
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.01.2017
Public Library of Science (PLoS)
Subjects
Acclimatization - genetics
Biology and Life Sciences
Cloning
Colleges & universities
Crops, Agricultural - genetics
Crops, Agricultural - growth & development
Funding
Gene Expression Regulation, Plant
Genetic aspects
Histones - genetics
Histones - metabolism
Laboratories
Oryza - genetics
Oryza - growth & development
Physiological aspects
Physiology
Plant Proteins - genetics
Plant Proteins - metabolism
Plant reproduction
Plant sciences
Polymorphism, Single Nucleotide
Protein Binding
Proteins
Research and Analysis Methods
Rice
Transcription (Genetics)
Transcription Factors - genetics
Transcription Factors - metabolism
Yeast
Italy
Online AccessGet full text

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Abstract Rice flowering is controlled by changes in the photoperiod that promote the transition to the reproductive phase as days become shorter. Natural genetic variation for flowering time has been largely documented and has been instrumental to define the genetics of the photoperiodic pathway, as well as providing valuable material for artificial selection of varieties better adapted to local environments. We mined genetic variation in a collection of rice varieties highly adapted to European regions and isolated distinct variants of the long day repressor HEADING DATE 1 (Hd1) that perturb its expression or protein function. Specific variants allowed us to define novel features of the photoperiodic flowering pathway. We demonstrate that a histone fold domain scaffold formed by GRAIN YIELD, PLANT HEIGHT AND HEADING DATE 8 (Ghd8) and several NF-YC subunits can accommodate distinct proteins, including Hd1 and PSEUDO RESPONSE REGULATOR 37 (PRR37), and that the resulting OsNF-Y complex containing Hd1 can bind a specific sequence in the promoter of HEADING DATE 3A (Hd3a). Artificial selection has locally favored an Hd1 variant unable to assemble in such heterotrimeric complex. The causal polymorphism was defined as a single conserved lysine in the CCT domain of the Hd1 protein. Our results indicate how genetic variation can be stratified and explored at multiple levels, and how its description can contribute to the molecular understanding of basic developmental processes.
AbstractList Rice flowering is controlled by changes in the photoperiod that promote the transition to the reproductive phase as days become shorter. Natural genetic variation for flowering time has been largely documented and has been instrumental to define the genetics of the photoperiodic pathway, as well as providing valuable material for artificial selection of varieties better adapted to local environments. We mined genetic variation in a collection of rice varieties highly adapted to European regions and isolated distinct variants of the long day repressor HEADING DATE 1 (Hd1) that perturb its expression or protein function. Specific variants allowed us to define novel features of the photoperiodic flowering pathway. We demonstrate that a histone fold domain scaffold formed by GRAIN YIELD, PLANT HEIGHT AND HEADING DATE 8 (Ghd8) and several NF-YC subunits can accommodate distinct proteins, including Hd1 and PSEUDO RESPONSE REGULATOR 37 (PRR37), and that the resulting OsNF-Y complex containing Hd1 can bind a specific sequence in the promoter of HEADING DATE 3A (Hd3a). Artificial selection has locally favored an Hd1 variant unable to assemble in such heterotrimeric complex. The causal polymorphism was defined as a single conserved lysine in the CCT domain of the Hd1 protein. Our results indicate how genetic variation can be stratified and explored at multiple levels, and how its description can contribute to the molecular understanding of basic developmental processes.
  Rice flowering is controlled by changes in the photoperiod that promote the transition to the reproductive phase as days become shorter. Natural genetic variation for flowering time has been largely documented and has been instrumental to define the genetics of the photoperiodic pathway, as well as providing valuable material for artificial selection of varieties better adapted to local environments. We mined genetic variation in a collection of rice varieties highly adapted to European regions and isolated distinct variants of the long day repressor HEADING DATE 1 (Hd1) that perturb its expression or protein function. Specific variants allowed us to define novel features of the photoperiodic flowering pathway. We demonstrate that a histone fold domain scaffold formed by GRAIN YIELD, PLANT HEIGHT AND HEADING DATE 8 (Ghd8) and several NF-YC subunits can accommodate distinct proteins, including Hd1 and PSEUDO RESPONSE REGULATOR 37 (PRR37), and that the resulting OsNF-Y complex containing Hd1 can bind a specific sequence in the promoter of HEADING DATE 3A (Hd3a). Artificial selection has locally favored an Hd1 variant unable to assemble in such heterotrimeric complex. The causal polymorphism was defined as a single conserved lysine in the CCT domain of the Hd1 protein. Our results indicate how genetic variation can be stratified and explored at multiple levels, and how its description can contribute to the molecular understanding of basic developmental processes.
Rice flowering is controlled by changes in the photoperiod that promote the transition to the reproductive phase as days become shorter. Natural genetic variation for flowering time has been largely documented and has been instrumental to define the genetics of the photoperiodic pathway, as well as providing valuable material for artificial selection of varieties better adapted to local environments. We mined genetic variation in a collection of rice varieties highly adapted to European regions and isolated distinct variants of the long day repressor HEADING DATE 1 (Hd1) that perturb its expression or protein function. Specific variants allowed us to define novel features of the photoperiodic flowering pathway. We demonstrate that a histone fold domain scaffold formed by GRAIN YIELD, PLANT HEIGHT AND HEADING DATE 8 (Ghd8) and several NF-YC subunits can accommodate distinct proteins, including Hd1 and PSEUDO RESPONSE REGULATOR 37 (PRR37), and that the resulting OsNF-Y complex containing Hd1 can bind a specific sequence in the promoter of HEADING DATE 3A (Hd3a). Artificial selection has locally favored an Hd1 variant unable to assemble in such heterotrimeric complex. The causal polymorphism was defined as a single conserved lysine in the CCT domain of the Hd1 protein. Our results indicate how genetic variation can be stratified and explored at multiple levels, and how its description can contribute to the molecular understanding of basic developmental processes.Rice flowering is controlled by changes in the photoperiod that promote the transition to the reproductive phase as days become shorter. Natural genetic variation for flowering time has been largely documented and has been instrumental to define the genetics of the photoperiodic pathway, as well as providing valuable material for artificial selection of varieties better adapted to local environments. We mined genetic variation in a collection of rice varieties highly adapted to European regions and isolated distinct variants of the long day repressor HEADING DATE 1 (Hd1) that perturb its expression or protein function. Specific variants allowed us to define novel features of the photoperiodic flowering pathway. We demonstrate that a histone fold domain scaffold formed by GRAIN YIELD, PLANT HEIGHT AND HEADING DATE 8 (Ghd8) and several NF-YC subunits can accommodate distinct proteins, including Hd1 and PSEUDO RESPONSE REGULATOR 37 (PRR37), and that the resulting OsNF-Y complex containing Hd1 can bind a specific sequence in the promoter of HEADING DATE 3A (Hd3a). Artificial selection has locally favored an Hd1 variant unable to assemble in such heterotrimeric complex. The causal polymorphism was defined as a single conserved lysine in the CCT domain of the Hd1 protein. Our results indicate how genetic variation can be stratified and explored at multiple levels, and how its description can contribute to the molecular understanding of basic developmental processes.
Rice flowering is controlled by changes in the photoperiod that promote the transition to the reproductive phase as days become shorter. Natural genetic variation for flowering time has been largely documented and has been instrumental to define the genetics of the photoperiodic pathway, as well as providing valuable material for artificial selection of varieties better adapted to local environments. We mined genetic variation in a collection of rice varieties highly adapted to European regions and isolated distinct variants of the long day repressor HEADING DATE 1 ( Hd1 ) that perturb its expression or protein function. Specific variants allowed us to define novel features of the photoperiodic flowering pathway. We demonstrate that a histone fold domain scaffold formed by GRAIN YIELD, PLANT HEIGHT AND HEADING DATE 8 (Ghd8) and several NF-YC subunits can accommodate distinct proteins, including Hd1 and PSEUDO RESPONSE REGULATOR 37 (PRR37), and that the resulting OsNF-Y complex containing Hd1 can bind a specific sequence in the promoter of HEADING DATE 3A ( Hd3a ). Artificial selection has locally favored an Hd1 variant unable to assemble in such heterotrimeric complex. The causal polymorphism was defined as a single conserved lysine in the CCT domain of the Hd1 protein. Our results indicate how genetic variation can be stratified and explored at multiple levels, and how its description can contribute to the molecular understanding of basic developmental processes. Many plant species flower in response to changes in day length and can be categorized depending on their requirements for long or short days. Rice has tropical origins and normally flowers in response to shortening days. However, artificial selection operated by ancient farmers or modern breeders adapted rice cultivation to several environments, including those typical of temperate regions characterized by long days during the cropping season. Modifications of the genetic network controlling flowering that are causal to such expansion have been the subject of extensive studies, but the full complement of genes that regulate it and the molecular bases of their activity remains unknown. We took advantage of germplasm cultivated in Europe—and highly adapted to flower under long days–to isolate widespread variants of the HEADING DATE 1 ( Hd1 ) gene that limits flowering in temperate areas, and showed that such variants are non-functional and unable to prevent long day flowering. We identified the DNA changes causing the gene to be non-functional and used such mutant alleles as tools to demonstrate that Hd1 can bind a specific DNA sequence in the promoter of a florigenic rice gene. Mining genetic diversity becomes thus instrumental to define the molecular properties of regulatory pathways.
Audience Academic
Author Gómez-Ariza, Jorge
Landini, Martina
Goretti, Daniela
Terauchi, Ryohei
Takagi, Hiroki
Collani, Silvio
Fornara, Fabio
Martignago, Damiano
Brambilla, Vittoria
Galbiati, Francesca
Gnesutta, Nerina
Mantovani, Roberto
AuthorAffiliation 5 Iwate Biotechnology Research Center and Laboratory of Crop Evolution, Graduate School of Agricultural Sciences, Kyoto University, Mozume, Muko, Kyoto, Japan
3 Department of Plant Biology and Crop Science, Rothamsted Research, Harpenden, United Kingdom
2 Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, Sweden
Chinese Academy of Agricultural Sciences, CHINA
1 Department of Biosciences, University of Milan, Via Celoria 26, Milan, Italy
4 Department of Agricultural and Environmental Sciences–Production, Territory, Agroenergy, University of Milan, Via Celoria 2, Milan, Italy
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– name: Chinese Academy of Agricultural Sciences, CHINA
– name: 3 Department of Plant Biology and Crop Science, Rothamsted Research, Harpenden, United Kingdom
– name: 5 Iwate Biotechnology Research Center and Laboratory of Crop Evolution, Graduate School of Agricultural Sciences, Kyoto University, Mozume, Muko, Kyoto, Japan
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/28068345$$D View this record in MEDLINE/PubMed
https://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-132845$$DView record from Swedish Publication Index
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ContentType Journal Article
Copyright COPYRIGHT 2017 Public Library of Science
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Goretti D, Martignago D, Landini M, Brambilla V, Gómez-Ariza J, Gnesutta N, et al. (2017) Transcriptional and Post-transcriptional Mechanisms Limit Heading Date 1 (Hd1) Function to Adapt Rice to High Latitudes. PLoS Genet 13(1): e1006530. doi:10.1371/journal.pgen.1006530
2017 Goretti et al 2017 Goretti et al
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Goretti D, Martignago D, Landini M, Brambilla V, Gómez-Ariza J, Gnesutta N, et al. (2017) Transcriptional and Post-transcriptional Mechanisms Limit Heading Date 1 (Hd1) Function to Adapt Rice to High Latitudes. PLoS Genet 13(1): e1006530. doi:10.1371/journal.pgen.1006530
Copyright_xml – notice: COPYRIGHT 2017 Public Library of Science
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Goretti D, Martignago D, Landini M, Brambilla V, Gómez-Ariza J, Gnesutta N, et al. (2017) Transcriptional and Post-transcriptional Mechanisms Limit Heading Date 1 (Hd1) Function to Adapt Rice to High Latitudes. PLoS Genet 13(1): e1006530. doi:10.1371/journal.pgen.1006530
– notice: 2017 Goretti et al 2017 Goretti et al
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Goretti D, Martignago D, Landini M, Brambilla V, Gómez-Ariza J, Gnesutta N, et al. (2017) Transcriptional and Post-transcriptional Mechanisms Limit Heading Date 1 (Hd1) Function to Adapt Rice to High Latitudes. PLoS Genet 13(1): e1006530. doi:10.1371/journal.pgen.1006530
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DocumentTitleAlternate Limiting Hd1 Function for Rice Adaptation
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Conceptualization: FF DG.Formal analysis: DG DM VB JGA SC HT RT.Funding acquisition: FF.Investigation: DG DM ML VB JGA NG.Methodology: FF DG DM NG SC HT RT RM FF.Project administration: FF.Resources: FF.Software: HT RT.Supervision: FF.Visualization: DG.Writing – original draft: DG RM FF.Writing – review & editing: FF.
The authors have declared that no competing interests exist.
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Snippet Rice flowering is controlled by changes in the photoperiod that promote the transition to the reproductive phase as days become shorter. Natural genetic...
  Rice flowering is controlled by changes in the photoperiod that promote the transition to the reproductive phase as days become shorter. Natural genetic...
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StartPage e1006530
SubjectTerms Acclimatization - genetics
Biology and Life Sciences
Cloning
Colleges & universities
Crops, Agricultural - genetics
Crops, Agricultural - growth & development
Funding
Gene Expression Regulation, Plant
Genetic aspects
Histones - genetics
Histones - metabolism
Laboratories
Oryza - genetics
Oryza - growth & development
Physiological aspects
Physiology
Plant Proteins - genetics
Plant Proteins - metabolism
Plant reproduction
Plant sciences
Polymorphism, Single Nucleotide
Protein Binding
Proteins
Research and Analysis Methods
Rice
Transcription (Genetics)
Transcription Factors - genetics
Transcription Factors - metabolism
Yeast
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Title Transcriptional and Post-transcriptional Mechanisms Limit Heading Date 1 (Hd1) Function to Adapt Rice to High Latitudes
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http://dx.doi.org/10.1371/journal.pgen.1006530
Volume 13
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