Identification of Genes Differentially Expressed in Response to Cold in Pisum sativum Using RNA Sequencing Analyses
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials, Experimental Design, and Cold Stress
2.2. RNA Extraction and High Throughput Sequencing
2.3. RNA-Sequencing Analysis, Assembly, and Annotation
2.4. Differential Expression Analysis and Statistical Tools
2.5. Statistical Differentially Expressed Genes (DEGs) Corroboration
3. Results
3.1. Samples, Sequencing, and Assembly Assessment
3.2. Differential Expression Analysis and Clustering
3.3. Functional Annotation, Gene Ontology (GO) Term Enrichment, and Kyoto Encyclopedia of Genes and Genomes (KEGG) Pathways
4. Discussion
4.1. Differences in Gene Expression Between The Two Lines Independently of the LT Treatment: Predispositions to Face Cold Stress?
4.2. How Pea Faces Cold Stress
4.2.1. Chilling Response
4.2.2. Champagne Specific Responses to Cold and Acquisition of Freezing Tolerance
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Set | Subset Description | # Genes | 5 Most Significant Enriched GO Terms Related to Biological Process | 5 Most Significant Enriched GO Terms Related to Cellular Localization | Kegg Pathways: # Mapped Genes (%), # Represented Pathways, Most Represented Pathways (#) | iTak: # Kinases (%), # Families | Transcription Factors: # TF (%), # Families, Most Represented Family (#) | GO Terms Related to Cold: # Genes |
---|---|---|---|---|---|---|---|---|
Line response (LR): genes differentially expressed between Ch and Te at T0 and not modulated under LT | Genes more expressed in Ch than in Te (Figure 3A a) | 906 | metabolic process, cellular process, localization, cellular component organization or biogenesis, response to stimulus | plastid, chloroplast cytoplasmic part, cell part, cell | 553 (61.0%), 110, Cysteine and methionine metabolism (13) | 26 (3.0%), 12 | 50 (5.5%), 26, AP2-EREBP (6) | -response to cold GO:0009409: 23 -cold acclimation GO:0009631: 4 -cellular response to cold GO:0070417: 2 -total: 29 (3.2%) |
Genes more expressed in Te than in Ch(Figure 3A b) | 1581 | cellular process, metabolic process, localization, cellular component organization or biogenesis, response to stimulus | cell part, cell, intracellular part, intracellular and intracellular organelle | 616 (39.0%), 106, Ribosome (25) | 70 (4.4%), 19 | 138 (8.7%) 43, bHLH (13) | -response to cold GO:0009409: 35 -cellular response to cold GO:0070417: 1 -total: 36 (2.3%) | |
Temperature Common Response (TCR): Genes responding identically in Ch and Te under LT | Genes down expressed during LT (Figure 3B a) | 520 | metabolic process, cellular process, cellular component organization or biogenesis, localization, response to stimulus | chloroplast, plastid, chloroplast part, plastid part, cytoplasm | 366 (70.4%), 77, Glyoxylate and dicarboxylate metabolism (10) | 16 (3.1%), 12 | 25 (4.8%), 16, bHLH (4) | -response to cold GO:0009409: 14 -Total: 14 (2.7%) |
Genes up expressed during LT (Figure 3B b) | 883 | metabolic process, cellular process, cellular component organization or biogenesis, localization, response to stimulus | intracellular, intracellular part, cell part, cell, membrane-bounded organelle | 388 (43.9%), 88, Ribosome biogenesis (21) | 38 (4.3%), 22 | 89 (10.1%), 38, bHLH (7), C2C2-CO-like (7) | -response to cold GO:0009409: 25 -cold acclimation GO:0009631: 3 -cellular response to cold GO:0070417: 2 -total: 30 (3.4%) | |
Temperature Line Specific Response (TLSR): genes responding differentially in Ch and Te under LT | Genes more expressed in Ch than in Te and down regulated during LT (Figure 3C a) | 253 | metabolic process, cellular process, localization, cellular component organization or biogenesis, response to stimulus | cytoplasmic part, plastid, chloroplast, cytoplasm, intracellular organelle part | 201 (79.5%), 73, Oxidative phosphorylation (6), Starch and sucrose metabolism (6) | 7 (2.8%), 6 | 16 (6.3%), 10, C3H (3), MYB (3) | -response to cold GO:0009409: 8 -cold acclimation GO:0009631: 1 -total: 9 (3.6%) |
Genes more expressed in Ch than in Te and up regulated during LT (Figure 3C b) | 228 | cellular process, metabolic process, localization, response to stimulus, cellular component organization or biogenesis | cell part, cell, intracellular part, cytoplasm, intracellular | 170 (74.6%), 62, Purine metabolism (5) | 11 (4.8%), 10 | 21 (9.2%), 15, AP2-EREBP (3) | -response to cold GO:0009409: 4 -cold acclimation GO:0009631: 1 -cellular response to cold GO:0070417: 1 -total: 6 (2.6%) | |
Genes less expressed in Ch than in Te and down regulated during LT (Figure 3C c) | 131 | metabolic process, cellular process, localization, response to stimulus, cellular component organization or biogenesis | cytoplasmic part | 57 (43.5%), 34, several pathways represented by 2 genes | 2 (1.5%), 2 | 12 (9.2%), 11, AP2-EREBP (2) | -response to cold GO:0009409: 8 -cold acclimation GO:0009631: 1 -total: 9 (6.9%) | |
Genes less expressed in Ch than in Te and up regulated during LT (Figure 3C d) | 479 | metabolic process, cellular process, localization, cellular component organization or biogenesis, response to stimulus | cell part, cell, intracellular part, intracellular, nucleus | 173 (36.1%), 71, mRNA surveillance pathway (7) | 23 (4.8%), 16 | 46 (9.6%), 25, C2H2 (5) | -response to cold GO:0009409: 11 -cold acclimation GO:0009631: 1 -total: 12 (2.5%) |
Protein/Gene/Function | Class of Function | Reference | Orthologous in AT | Ch Up | Te Up | TCR Down | TCR Up | TLSR a | TLSR b | TLSR c | TLSR d |
---|---|---|---|---|---|---|---|---|---|---|---|
GO:0009409 (response to cold) | |||||||||||
Calmodulin-binding transcription activator 2 | TF, Induction of CBFs | [53] | AT5G64220.2 | 1 | |||||||
Plasma-membrane cation-binding protein 1 | Plasma membrane protein | [54] | AT4G20260.6 | 1 | |||||||
Vacuolar H(+)-ATPase subunit E1 | Hydrogen ion transport | [54] | AT4G11150.1 | 1 | |||||||
Adenine nucleotide alpha hydrolases-like | Cold shock response | [54] | AT3G53990.1 | 2 | |||||||
Calcium-dependent lipid-binding protein | Response to cold | [54] | AT4G34150.1 | 1 | |||||||
SAUR-like auxin-responsive protein family | Auxin metabolism | [55] | AT4G38840.1 | 4 | 4 | ||||||
Enolase, ENO2 | Glycolysis/Gluconeogenesis | [56] | AT2G36530.1 | 1 | |||||||
MAP kinase kinase kinase1 | Kinase activity | [57] | AT4G08500.1 | 1 | |||||||
Protein HAPLESS 6, Ribophorin II | N-linked glycosylation | [58] | AT4G21150.3 | 1 | |||||||
Cold, circadian rhythm, RNA-binding 2, GRP7 | RNA-binding | [59] | AT2G21660.2 | 5 | 5 | 5 | |||||
Glycine-rich RNA-binding protein 3, RBG3 | RNA-binding, transcription | [59] | AT5G61030.1 | 2 | |||||||
Hydrophobic protein RCI2A and LTI6A | Response to cold | [60] | AT3G05880.1 | 2 | |||||||
Late embryogenesis abundant protein 46 | Cryoprotectant | [61] | AT5G06760.1 | 1 | |||||||
Galactinol synthase 2, GOLS2 | Galactose metabolism | [62] | AT1G56600.1 | 1 | |||||||
Protein sensitive to freezing 2 | Glucosidase activity | [63] | AT3G06510.1 | 1 | |||||||
Pentatricopeptide repeat-containing protein | RNA modification, binding | [64] | AT3G22690.2 | 1 | |||||||
RNA-binding (RRM/RBD/RNP motifs) | rRNA-binding | [64] | AT1G70200.1 | 1 | |||||||
Outer envelope pore protein 16-1, OEP16-1 | Amino acid transport, porin | [65] | AT2G28900.1 | 2 | 2 | ||||||
Glutathione S-transferase F8 | Oxidoreductase, peroxidase | [66] | AT2G47730.1 | 1 | |||||||
Glyoxalase I | methylglyoxal degradation | [66] | AT1G67280.2 | 2 | |||||||
Plastid-lipid-associated protein 1, Fibrillin-1a | Photoinhibition | [66] | AT4G04020.1 | 1 | |||||||
Phosphoribulokinase, PRK | Photosynthesis, transferase | [66] | AT1G32060.1 | 1 | |||||||
NADPH-dependent alkenal/one | Oxidoreductase | [66] | AT1G23740.1 | 2 | 2 | ||||||
Serine hydroxymethyltransferase | One-carbon metabolism | [66] | AT4G37930.1 | 1 | |||||||
RuBisCo activase | ATP- and nucleotide-binding | [66] | AT2G39730.1 | 1 | |||||||
Chlorophyll a-b binding protein 4, LHCA4 | Photosynthesis | [67] | AT3G47470.1 | 1 | 1 | ||||||
NADPH-dependent aldo-keto reductase | Oxidation-reduction process | [68] | AT2G37770.2 | 2 | 2 | ||||||
3-hydroxyisobutyryl-CoA hydrolase 1 | L-valine degradation | [69] | AT5G65940.1 | 1 | |||||||
PLAT domain-containing protein 1, PLAT1 | Catalase, Peroxidase activity | [70] | AT4G39730.1 | 2 | 2 | ||||||
Serine/threonine protein kinase | ATP binding, transferase | [71] | AT3G08720.2 | 1 | |||||||
Phosphoglyceromutase 1, PGAM 1 | Glycolysis/Gluconeogenesis | [72] | AT1G09780.1 | 1 | |||||||
3-ketoacyl-CoA synthase 1 | Fatty acid elongation | [73] | AT2G26250.1 | 1 | 2 | 2 | |||||
Acyl-CoA-binding protein 1, ACBP1 | Fatty Acid Beta-Oxidation | [74] | AT5G53470.1 | 1 | 1 | ||||||
Agamous-like MADS-box protein, SOC1 | Transcription regulation | [75] | AT2G45660.1 | 2 | |||||||
Alcohol dehydrogenase 1 | Glycolysis/Gluconeogenesis | [76] | AT1G77120.1 | 1 | |||||||
Annexin D8, calcium/phospholipid binding | Calcium binding | [77] | AT5G12380.1 | 1 | 1 | 1 | |||||
BAG family molecular chaperone regulator 4 | Chaperone binding | [78] | AT3G51780.1 | 1 | |||||||
Calcium-binding protein | Calcium ion binding | [79] | AT1G02270.1 | 1 | |||||||
Heat shock 70 KDa protein 1, HSP70-1 | ATPase activity, chaperone | [79] | AT5G02500.1 | 2 | |||||||
DNA damage-repair/toleration, DRT102 | Isomerase activity | [79] | AT3G04880.1 | 1 | |||||||
Proteasome subunit alpha type-3, PAG1 | Folding, sorting, degradation | [79] | AT2G27020.1 | 1 | |||||||
Hsp 70 kDa protein 1 | ATPase activity, Chaperone | [79] | AT5G02500.1 | 2 | |||||||
Calmodulin-binding receptor-like, kinase 1 | Calmodulin binding | [80] | AT5G58940.1 | 1 | |||||||
Serine/threonine-protein kinase | ATP-binding | [81] | AT1G01140.3 | 1 | |||||||
Chaperonin-like RBCX protein 1 | Protein folding chaperone | [82] | AT4G04330.1 | 1 | |||||||
Cinnamoyl-CoA reductase 1 | Lignin biosynthesis | [83] | AT1G15950.1 | 1 | |||||||
Cold regulated protein 27, COR27 | Cold, circadian rhythm | [84] | AT5G42900.3 | 1 | |||||||
Cysteine proteinase inhibitor 6, CYS6 | Cysteine proteinase inhibitor | [85] | AT3G12490.2 | 1 | |||||||
Protein CRYOPHYTE, RH38 | RNA-binding, hydrolase | [86] | AT3G53110.1 | 1 | |||||||
Diacylglycerol kinase 2 | Glycerolipid metabolism | [87] | AT5G63770.1 | 1 | |||||||
E3 ubiquitin-protein ligase HOS1 | Protein ubiquitination | [88] | AT2G39810.1 | 1 | |||||||
Early light-induced protein 1, Chloroplastic | Photosynthesis | [89] | AT3G22840.1 | 1 | |||||||
Ethylene-responsive TF, RAP2-4 and RAP2 | Transcription factor | [90] | AT1G78080.1 | 1 | 1 | ||||||
Glycine-rich RNA-binding protein RZ1A | RNA-binding, transcription | [91] | AT3G26420.1 | 1 | 1 | ||||||
HVA22-like protein a, similarity to TB2/DP1 | Cold and stress response | [92] | AT1G74520.1 | 1 | 1 | ||||||
Inositol-1-monophosphatase | Myo-inositol biosynthesis | [93] | AT3G02870.3 | 1 | |||||||
Lipid transfer protein EARLI 1 | Lipid-transfer | [94] | AT4G12480.1 | 1 | |||||||
LOW-TEMPERATURE-INDUCED 65, LTI65 | Response to abscisic acid | [95] | AT5G52300.2 | 1 | |||||||
MAP kinase 3 | ATP binding | [96] | AT3G45640.1 | 1 | |||||||
MYB-related transcription factor CCA1 | DNA binding | [97] | AT2G46830.1 | 2 | |||||||
Phosphoinositide phospholipase C1 | Hydrolase, lipid metabolism | [98] | AT5G58670.1 | 1 | |||||||
Phospholipase D delta | Lipid degradation | [99] | AT4G35790.2 | 2 | 2 | ||||||
Protein EARLY FLOWERING 3, ELF3 | DNA-binding TF activity | [100] | AT2G25930.1 | 1 | |||||||
Protein ESKIMO 1, Signal-anchor | Xylan O-acetyltransferase | [101] | AT3G55990.1 | 1 | |||||||
Protein GIGANTEA, GI | Phytochrome B signaling | [102] | AT1G22770.1 | 1 | |||||||
Protein Senescence-Associated Gene 21 | Oxidative stresses | [103] | AT4G02380.1 | 2 | |||||||
Raffinose synthase 6 | Carbohydrate metabolism | [104] | AT5G20250.4 | 1 | |||||||
Synaptotagmin-1, SYT1 | Lipid binding, Ca2+ transport | [105] | AT2G20990.1 | 1 | |||||||
Transcription factor GTE10, NPX1 | ABA signaling pathway | [106] | AT5G63320.1 | 1 | |||||||
Tubulin beta-6 chain, TUBB6 | GTPase activity, Transport | [107] | AT5G12250.1 | 1 | |||||||
WRKY DNA-binding protein 33, WRKY33 | DNA-binding TF activity | [108] | AT2G38470.1 | 1 | |||||||
Xyloglucan endotransglucosylase/hydrolase protein 22 | Glycosidase, Transferase | [109] | AT5G57560.1 | 1 | |||||||
GO:0009631 (cold acclimation) | |||||||||||
Cold-regulated 413 thylakoid membrane 1 | Cellular response to cold | [110] | AT1G29395.1 | 1 | |||||||
3-oxoacyl-[acyl-carrier-protein] synthase II | Fatty acid biosynthesis | [111] | AT1G74960.3 | 1 | |||||||
Mediator of RNA polymerase II transcription subunit 32 | Transcription regulation | [112] | AT1G11760.1 | 1 | |||||||
Calcium/calmodulin-regulated receptor-like kinase 1 | Calmodulin-binding | [113] | AT5G54590.2 | 1 | |||||||
Alpha-glucan water dikinase 1 | Carbohydrate metabolism | [114] | AT1G10760.1 | 1 | |||||||
Transcriptional adapter ADA2b, PRZ1 | Transcription regulation | [115] | AT4G16420.1 | 1 | |||||||
Glycine-rich RNA-binding protein 2 | Chaperone, RNA-binding | [116] | AT4G13850.3 | 1 | |||||||
Acetyl-CoA carboxylase 1 | Fatty acid metabolism | [117] | AT1G36160.2 | 1 | |||||||
C-repeat binding factor 3, DREB1A, CBF3 | TF, DNA-binding | [118] | AT4G25480.1 | 1 | |||||||
VOZ1, vascular plant one zinc finger | Transcription factor | [119] | AT1G28520.2 | 1 | |||||||
GO:0070417 (cellular response to cold) | |||||||||||
Pre-mRNA-processing factor 31 homolog | RNA-binding, splicing | [120] | AT1G60170.1 | 1 | |||||||
Bidirectional sugar transporter SWEET17 | Fructose, sugar transport | [121] | AT4G15920.1 | 1 | |||||||
Delta(8)-fatty-acid desaturase1 | Oxidoreductase | [122] | AT2G46210.1 | 1 | 1 | ||||||
Glutamate receptor 3.4, GLR3.4 | Ion transport | [123] | AT1G05200.2 | 1 | |||||||
Organic cation/carnitine transporter 3, OCT3 | Transporter activity | [124] | AT1G16390.1 | 1 | |||||||
spliceosome protein-like protein | RNA processing, splicing | [125] | AT1G54380.1 | 1 | |||||||
Total of genes in GO bulk analyses | 29 | 36 | 14 | 30 | 9 | 6 | 9 | 12 | |||
Total of genes in each subset | 906 | 1581 | 520 | 883 | 253 | 228 | 131 | 479 | |||
Ratio % | 3.20 | 2.28 | 2.69 | 3.40 | 3.56 | 2.63 | 6.87 | 2.51 |
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Bahrman, N.; Hascoët, E.; Jaminon, O.; Dépta, F.; Hû, J.-F.; Bouchez, O.; Lejeune-Hénaut, I.; Delbreil, B.; Legrand, S. Identification of Genes Differentially Expressed in Response to Cold in Pisum sativum Using RNA Sequencing Analyses. Plants 2019, 8, 288. https://doi.org/10.3390/plants8080288
Bahrman N, Hascoët E, Jaminon O, Dépta F, Hû J-F, Bouchez O, Lejeune-Hénaut I, Delbreil B, Legrand S. Identification of Genes Differentially Expressed in Response to Cold in Pisum sativum Using RNA Sequencing Analyses. Plants. 2019; 8(8):288. https://doi.org/10.3390/plants8080288
Chicago/Turabian StyleBahrman, Nasser, Emilie Hascoët, Odile Jaminon, Frédéric Dépta, Jean-François Hû, Olivier Bouchez, Isabelle Lejeune-Hénaut, Bruno Delbreil, and Sylvain Legrand. 2019. "Identification of Genes Differentially Expressed in Response to Cold in Pisum sativum Using RNA Sequencing Analyses" Plants 8, no. 8: 288. https://doi.org/10.3390/plants8080288