Transcriptome profiling of Ricinus communis L. provides new insights underlying the mechanisms towards thermotolerance during seed imbibition and germination

Paulo R. Ribeiro*, Leo A.J. Willems, Anderson T. Silva, Luzimar G. Fernandez, Renato D. de Castro, Johan Bucher, Basten L. Snoek, Henk W.M. Hilhorst, Wilco Ligterink

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Ricinus communis seeds germinate to a high percentage and faster at 35 °C than at lower temperatures, but with compromised seedling establishment and survival. However, seedlings are able to cope with high temperatures at later stages of seedling establishment if germination occurred at lower temperatures. The identification of this thermo-sensitive window during seed germination suggests that temperature disturb crucial mechanisms that support seedling establishment. We studied the molecular mechanisms that could explain this thermo-sensitive window with a genomics approach using microarray analysis to determine transcriptome changes during seed germination at 20, 25 and 35 °C. Although temperature had a strong effect on the R. communis transcriptome, most of these differences occurred between 6 h of imbibition and the commencement of germination, i.e. radicle protrusion, which coincided with the identified thermo-sensitive window. We identified several responsive genes that might be involved in the thermotolerance of R. communis. Temperature had a major effect on genes involved in energy generating pathways, such as the Calvin-Benson-Bassham cycle, gluconeogenesis, and starch- and triacylglycerol degradation. Transcripts of ATP binding proteins, DNA binding proteins, RNA binding proteins, DNA-directed RNA polymerases, heat shock factor proteins, multiprotein-bridging factor proteins, and zinc finger proteins were also affected by temperature suggesting that transcriptional reprogramming mechanisms were disturbed. Among the downregulated transcripts, three were shared by all three stages: one oxidation-related zinc finger 2, one F-box and wd40 domain protein, and one DNA binding protein/ MYB-like transcription factor. Among the upregulated transcripts, nine were shared by all three stages: one BET1P/SFT1P-like protein 14BB, one low-molecular-weight cysteine-rich protein LCR78, one WD-repeat protein, one GAST1 protein, one adenylate kinase 1/P-loop containing nucleoside triphosphate hydrolases superfamily protein, and four conserved hypothetical proteins. These genes constitute good candidate genes for further characterization of temperature-responsive molecular mechanisms in R. communis, which in turn will provide necessary tools for the exploitation of R. communis by small family farmers under the typical harsh conditions of semiarid regions worldwide.

Original languageEnglish
Pages (from-to)380-393
JournalIndustrial Crops and Products
Volume126
Early online date20 Oct 2018
DOIs
Publication statusPublished - 15 Dec 2018

Fingerprint

Ricinus communis
imbibition
transcriptomics
heat tolerance
germination
seeds
proteins
temperature
DNA-binding proteins
seedlings
zinc finger motif
transcriptome
seed germination
genes
adenylate kinase
RNA-binding proteins
gluconeogenesis
Calvin cycle
nucleosides
semiarid zones

Keywords

  • Cytochrome P450s
  • Heat shock proteins
  • Heat stress
  • Microarray analysis
  • Transcriptional regulation

Cite this

@article{573455b10c1441359ab3700c1dff99bc,
title = "Transcriptome profiling of Ricinus communis L. provides new insights underlying the mechanisms towards thermotolerance during seed imbibition and germination",
abstract = "Ricinus communis seeds germinate to a high percentage and faster at 35 °C than at lower temperatures, but with compromised seedling establishment and survival. However, seedlings are able to cope with high temperatures at later stages of seedling establishment if germination occurred at lower temperatures. The identification of this thermo-sensitive window during seed germination suggests that temperature disturb crucial mechanisms that support seedling establishment. We studied the molecular mechanisms that could explain this thermo-sensitive window with a genomics approach using microarray analysis to determine transcriptome changes during seed germination at 20, 25 and 35 °C. Although temperature had a strong effect on the R. communis transcriptome, most of these differences occurred between 6 h of imbibition and the commencement of germination, i.e. radicle protrusion, which coincided with the identified thermo-sensitive window. We identified several responsive genes that might be involved in the thermotolerance of R. communis. Temperature had a major effect on genes involved in energy generating pathways, such as the Calvin-Benson-Bassham cycle, gluconeogenesis, and starch- and triacylglycerol degradation. Transcripts of ATP binding proteins, DNA binding proteins, RNA binding proteins, DNA-directed RNA polymerases, heat shock factor proteins, multiprotein-bridging factor proteins, and zinc finger proteins were also affected by temperature suggesting that transcriptional reprogramming mechanisms were disturbed. Among the downregulated transcripts, three were shared by all three stages: one oxidation-related zinc finger 2, one F-box and wd40 domain protein, and one DNA binding protein/ MYB-like transcription factor. Among the upregulated transcripts, nine were shared by all three stages: one BET1P/SFT1P-like protein 14BB, one low-molecular-weight cysteine-rich protein LCR78, one WD-repeat protein, one GAST1 protein, one adenylate kinase 1/P-loop containing nucleoside triphosphate hydrolases superfamily protein, and four conserved hypothetical proteins. These genes constitute good candidate genes for further characterization of temperature-responsive molecular mechanisms in R. communis, which in turn will provide necessary tools for the exploitation of R. communis by small family farmers under the typical harsh conditions of semiarid regions worldwide.",
keywords = "Cytochrome P450s, Heat shock proteins, Heat stress, Microarray analysis, Transcriptional regulation",
author = "Ribeiro, {Paulo R.} and Willems, {Leo A.J.} and Silva, {Anderson T.} and Fernandez, {Luzimar G.} and {de Castro}, {Renato D.} and Johan Bucher and Snoek, {Basten L.} and Hilhorst, {Henk W.M.} and Wilco Ligterink",
year = "2018",
month = "12",
day = "15",
doi = "10.1016/j.indcrop.2018.10.024",
language = "English",
volume = "126",
pages = "380--393",
journal = "Industrial Crops and Products",
issn = "0926-6690",
publisher = "Elsevier",

}

Transcriptome profiling of Ricinus communis L. provides new insights underlying the mechanisms towards thermotolerance during seed imbibition and germination. / Ribeiro, Paulo R.; Willems, Leo A.J.; Silva, Anderson T.; Fernandez, Luzimar G.; de Castro, Renato D.; Bucher, Johan; Snoek, Basten L.; Hilhorst, Henk W.M.; Ligterink, Wilco.

In: Industrial Crops and Products, Vol. 126, 15.12.2018, p. 380-393.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Transcriptome profiling of Ricinus communis L. provides new insights underlying the mechanisms towards thermotolerance during seed imbibition and germination

AU - Ribeiro, Paulo R.

AU - Willems, Leo A.J.

AU - Silva, Anderson T.

AU - Fernandez, Luzimar G.

AU - de Castro, Renato D.

AU - Bucher, Johan

AU - Snoek, Basten L.

AU - Hilhorst, Henk W.M.

AU - Ligterink, Wilco

PY - 2018/12/15

Y1 - 2018/12/15

N2 - Ricinus communis seeds germinate to a high percentage and faster at 35 °C than at lower temperatures, but with compromised seedling establishment and survival. However, seedlings are able to cope with high temperatures at later stages of seedling establishment if germination occurred at lower temperatures. The identification of this thermo-sensitive window during seed germination suggests that temperature disturb crucial mechanisms that support seedling establishment. We studied the molecular mechanisms that could explain this thermo-sensitive window with a genomics approach using microarray analysis to determine transcriptome changes during seed germination at 20, 25 and 35 °C. Although temperature had a strong effect on the R. communis transcriptome, most of these differences occurred between 6 h of imbibition and the commencement of germination, i.e. radicle protrusion, which coincided with the identified thermo-sensitive window. We identified several responsive genes that might be involved in the thermotolerance of R. communis. Temperature had a major effect on genes involved in energy generating pathways, such as the Calvin-Benson-Bassham cycle, gluconeogenesis, and starch- and triacylglycerol degradation. Transcripts of ATP binding proteins, DNA binding proteins, RNA binding proteins, DNA-directed RNA polymerases, heat shock factor proteins, multiprotein-bridging factor proteins, and zinc finger proteins were also affected by temperature suggesting that transcriptional reprogramming mechanisms were disturbed. Among the downregulated transcripts, three were shared by all three stages: one oxidation-related zinc finger 2, one F-box and wd40 domain protein, and one DNA binding protein/ MYB-like transcription factor. Among the upregulated transcripts, nine were shared by all three stages: one BET1P/SFT1P-like protein 14BB, one low-molecular-weight cysteine-rich protein LCR78, one WD-repeat protein, one GAST1 protein, one adenylate kinase 1/P-loop containing nucleoside triphosphate hydrolases superfamily protein, and four conserved hypothetical proteins. These genes constitute good candidate genes for further characterization of temperature-responsive molecular mechanisms in R. communis, which in turn will provide necessary tools for the exploitation of R. communis by small family farmers under the typical harsh conditions of semiarid regions worldwide.

AB - Ricinus communis seeds germinate to a high percentage and faster at 35 °C than at lower temperatures, but with compromised seedling establishment and survival. However, seedlings are able to cope with high temperatures at later stages of seedling establishment if germination occurred at lower temperatures. The identification of this thermo-sensitive window during seed germination suggests that temperature disturb crucial mechanisms that support seedling establishment. We studied the molecular mechanisms that could explain this thermo-sensitive window with a genomics approach using microarray analysis to determine transcriptome changes during seed germination at 20, 25 and 35 °C. Although temperature had a strong effect on the R. communis transcriptome, most of these differences occurred between 6 h of imbibition and the commencement of germination, i.e. radicle protrusion, which coincided with the identified thermo-sensitive window. We identified several responsive genes that might be involved in the thermotolerance of R. communis. Temperature had a major effect on genes involved in energy generating pathways, such as the Calvin-Benson-Bassham cycle, gluconeogenesis, and starch- and triacylglycerol degradation. Transcripts of ATP binding proteins, DNA binding proteins, RNA binding proteins, DNA-directed RNA polymerases, heat shock factor proteins, multiprotein-bridging factor proteins, and zinc finger proteins were also affected by temperature suggesting that transcriptional reprogramming mechanisms were disturbed. Among the downregulated transcripts, three were shared by all three stages: one oxidation-related zinc finger 2, one F-box and wd40 domain protein, and one DNA binding protein/ MYB-like transcription factor. Among the upregulated transcripts, nine were shared by all three stages: one BET1P/SFT1P-like protein 14BB, one low-molecular-weight cysteine-rich protein LCR78, one WD-repeat protein, one GAST1 protein, one adenylate kinase 1/P-loop containing nucleoside triphosphate hydrolases superfamily protein, and four conserved hypothetical proteins. These genes constitute good candidate genes for further characterization of temperature-responsive molecular mechanisms in R. communis, which in turn will provide necessary tools for the exploitation of R. communis by small family farmers under the typical harsh conditions of semiarid regions worldwide.

KW - Cytochrome P450s

KW - Heat shock proteins

KW - Heat stress

KW - Microarray analysis

KW - Transcriptional regulation

U2 - 10.1016/j.indcrop.2018.10.024

DO - 10.1016/j.indcrop.2018.10.024

M3 - Article

VL - 126

SP - 380

EP - 393

JO - Industrial Crops and Products

JF - Industrial Crops and Products

SN - 0926-6690

ER -