Selection of transcripts related to low-temperature tolerance using RNA sequencing from F2 plants between japonica and indica rice (Oryza sativa L.) cultivars
Akari Fukuda
A E , Tatsuro Hirose B , Yoichi Hashida B , Naohiro Aoki C and Atsushi J. Nagano D
+ Author Affiliations
- Author Affiliations
A Institute of Crop Science, National Agriculture and Food Research Organization, Tsukuba, Ibaraki, Japan.
B Faculty of Agriculture, Takasaki University of Health and Welfare, Takasaki, Gunma, Japan.
C Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan.
D Faculty of Agriculture, Ryukoku University, Otsu, Shiga, Japan.
E Corresponding author. Email: akfukuda@affrc.go.jp
Functional Plant Biology 48(10) 984-993 https://doi.org/10.1071/FP21088
Submitted: 23 March 2021 Accepted: 21 May 2021 Published: 11 June 2021
Journal Compilation © CSIRO 2021 Open Access CC BY-NC-ND
Abstract
At low temperatures (18°C), seedlings of an indica rice (Oryza sativa L.) cultivar Kasalath showed symptoms of chlorosis, although the leaves of a japonica cultivar Arroz da Terra remained green. In this study, transcripts related to the chlorophyll content of rice seedlings grown at 18°C were investigated using RNA-sequencing (RNA-Seq) data for F2 crosses between cultivars Arroz da Terra and Kasalath, as well as their parental cultivars. Differential expression analysis revealed that gene ontology terms related to ‘photosynthesis’ were significantly enriched in lowly expressed genes at 18°C than at 25°C in Kasalath. However, the gene ontology terms related to ‘response to stress’ were significantly enriched in highly expressed genes at 18°C than at 25°C in Kasalath. When the F2 plants were grown at 18°C, their chlorophyll contents varied. Transcripts with expression levels related to chlorophyll content were statistically selected using RNA-Seq data from 21 F2 plants. In regression models, frequently selected genes included four photosynthetic and two stress-responsive genes. The expression values of four photosynthetic and two stress-responsive genes in high-frequency selected genes were significantly correlated with chlorophyll content not only in plants analysed using RNA-Seq but also in 95 F2 plants.
Keywords: cold tolerance, low temperature, LASSO, POX22.3, RNA sequencing (RNA-Seq), TIFY11C, transcriptome, rice, Oryza sativa L.
References
Ando T, Yamamoto T, Shimizu T, Ma XF, Shomura A, Takeuchi Y, Lin SY, Yano M (2008) Genetic dissection and pyramiding of quantitative traits for panicle architecture by using chromosomal segment substitution lines in rice. Theoretical and Applied Genetics 116, 881–890.| Genetic dissection and pyramiding of quantitative traits for panicle architecture by using chromosomal segment substitution lines in rice.Crossref | GoogleScholarGoogle Scholar | 18274726PubMed |
Bai LWD, Liu J, Dai LF, Deng QW, Chen YL, Xie JK, Luo XD (2021) Identification and characterisation of cold stress-related proteins in Oryza rufipogon at the seedling stage using label-free quantitative proteomic analysis. Functional Plant Biology 48, 542–555.
| Identification and characterisation of cold stress-related proteins in Oryza rufipogon at the seedling stage using label-free quantitative proteomic analysis.Crossref | GoogleScholarGoogle Scholar |
Buti M, Pasquariello M, Ronga D, Milc JA, Pecchioni N, Ho VT, Pucciariello C, Perata P, Francia E (2018) Transcriptome profiling of short-term response to chilling stress in tolerant and sensitive Oryza sativa ssp Japonica seedlings. Functional & Integrative Genomics 18, 627–644.
| Transcriptome profiling of short-term response to chilling stress in tolerant and sensitive Oryza sativa ssp Japonica seedlings.Crossref | GoogleScholarGoogle Scholar |
Chittoor JM, Leach JE, White FF (1997) Differential induction of a peroxidase gene family during infection of rice by Xanthomonas oryzae pv. oryzae. Molecular Plant-Microbe Interactions 10, 861–871.
| Differential induction of a peroxidase gene family during infection of rice by Xanthomonas oryzae pv. oryzae.Crossref | GoogleScholarGoogle Scholar | 9304860PubMed |
da Maia LC, Cadore PRB, Benitez LC, Danielowski R, Braga EJB, Fagundes PRR, Magalhaes AM, de Oliveira AC (2017) Transcriptome profiling of rice seedlings under cold stress. Functional Plant Biology 44, 419–429.
| Transcriptome profiling of rice seedlings under cold stress.Crossref | GoogleScholarGoogle Scholar | 32480575PubMed |
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Research 38, W64–W70.
| agriGO: a GO analysis toolkit for the agricultural community.Crossref | GoogleScholarGoogle Scholar | 20435677PubMed |
Friedman J, Hastie T, Tibshirani R (2010) Regularization paths for generalized linear models via coordinate descent. Journal of Statistical Software 33, 1–22.
| Regularization paths for generalized linear models via coordinate descent.Crossref | GoogleScholarGoogle Scholar | 20808728PubMed |
Fukuda A, Terao T (2015) QTLs for shoot length and chlorophyll content of rice seedlings grown under low-temperature conditions, using a cross between Indica and Japonica cultivars. Plant Production Science 18, 128–136.
| QTLs for shoot length and chlorophyll content of rice seedlings grown under low-temperature conditions, using a cross between Indica and Japonica cultivars.Crossref | GoogleScholarGoogle Scholar |
Fukuda A, Hirose T, Aoki N, Kondo S, Yonekura M, Kataoka T, Ohto C, Nagano AJ (2018) Selection of transcripts affecting initial growth rate of rice backcrossed inbred lines using RNA sequencing data. Frontiers in Plant Science 9, 1880
| Selection of transcripts affecting initial growth rate of rice backcrossed inbred lines using RNA sequencing data.Crossref | GoogleScholarGoogle Scholar | 30631334PubMed |
Hakata M, Muramatsu M, Nakamura H, Hara N, Kishimoto M, Iida-Okada K, Kajikawa M, Imai-Toki N, Toki S, Nagamura Y, Yamakawa H, Ichikawa H (2017) Overexpression of TIFY genes promotes plant growth in rice through jasmonate signaling. Bioscience, Biotechnology, and Biochemistry 81, 906–913.
| Overexpression of TIFY genes promotes plant growth in rice through jasmonate signaling.Crossref | GoogleScholarGoogle Scholar | 28079456PubMed |
Han B, Ma XD, Cui D, Wang YJ, Geng LY, Cao GL, Zhang H, Han LZ (2020) Comprehensive evaluation and analysis of the mechanism of cold tolerance based on the transcriptome of weedy rice seedlings. Rice (New York, N.Y.) 13, 12
| Comprehensive evaluation and analysis of the mechanism of cold tolerance based on the transcriptome of weedy rice seedlings.Crossref | GoogleScholarGoogle Scholar |
Huang GT, Ma SL, Bai LP, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo ZF (2012) Signal transduction during cold, salt, and drought stresses in plants. Molecular Biology Reports 39, 969–987.
| Signal transduction during cold, salt, and drought stresses in plants.Crossref | GoogleScholarGoogle Scholar | 21573796PubMed |
Huner NPA, Oquist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low-temperature acclimation in cold tolerant plants. Photosynthesis Research 37, 19–39.
| Photosynthesis, photoinhibition and low-temperature acclimation in cold tolerant plants.Crossref | GoogleScholarGoogle Scholar |
Kamitani M, Kashima M, Tezuka A, Nagano AJ (2019) Lasy-Seq: a high-throughput library preparation method for RNA-Seq and its application in the analysis of plant responses to fluctuating temperatures. Scientific Reports 9, 7091
| Lasy-Seq: a high-throughput library preparation method for RNA-Seq and its application in the analysis of plant responses to fluctuating temperatures.Crossref | GoogleScholarGoogle Scholar | 31068632PubMed |
Kersey PJ, Allen JE, Armean I, Boddu S, Bolt BJ, Carvalho-Silva D, Christensen M, Davis P, Falin LJ, Grabmueller C, Humphrey J, Kerhornou A, Khobova J, Aranganathan NK, Langridge N, Lowy E, McDowall MD, Maheswari U, Nuhn M, Ong CK, Overduin B, Paulini M, Pedro H, Perry E, Spudich G, Tapanari E, Walts B, Williams G, Tello-Ruiz M, Stein J, Wei S, Ware D, Bolser DM, Howe KL, Kulesha E, Lawson D, Maslen G, Staines DM (2016) Ensembl Genomes 2016: more genomes, more complexity. Nucleic Acids Research 44, D574–D580.
| Ensembl Genomes 2016: more genomes, more complexity.Crossref | GoogleScholarGoogle Scholar | 26578574PubMed |
Kodama Y, Shumway M, Leinonen R (2012) International Nucleotide Sequence Database Collaboration. The sequence read archive: explosive growth of sequencing data. Nucleic Acids Research 40, D54–D56.
| International Nucleotide Sequence Database Collaboration. The sequence read archive: explosive growth of sequencing data.Crossref | GoogleScholarGoogle Scholar | 22009675PubMed |
Kudapa H, Ramalingam A, Nayakoti S, Chen XP, Zhuang WJ, Liang XQ, Kahl G, Edwards D, Varshney RK (2013) Functional genomics to study stress responses in crop legumes: progress and prospects. Functional Plant Biology 40, 1221–1233.
| Functional genomics to study stress responses in crop legumes: progress and prospects.Crossref | GoogleScholarGoogle Scholar | 32481190PubMed |
Kumagai E, Araki T, Kubota F (2009) Correlation of chlorophyll meter readings with gas exchange and chlorophyll fluorescence in flag leaves of rice (Oryza sativa L.) Plants. Plant Production Science 12, 50–53.
| Correlation of chlorophyll meter readings with gas exchange and chlorophyll fluorescence in flag leaves of rice (Oryza sativa L.) Plants.Crossref | GoogleScholarGoogle Scholar |
Li M, Sui N, Lin L, Yang Z, Zhang YH (2019) Transcriptomic profiling revealed genes involved in response to cold stress in maize. Functional Plant Biology 46, 830–844.
| Transcriptomic profiling revealed genes involved in response to cold stress in maize.Crossref | GoogleScholarGoogle Scholar | 31217070PubMed |
Lv Y, Yang M, Hu D, Yang ZY, Ma SQ, Li XH, Xiong LZ (2017) The OsMYB30 transcription factor suppresses cold tolerance by interacting with a JAZ protein and suppressing β-amylase expression. Plant Physiology 173, 1475–1491.
| The OsMYB30 transcription factor suppresses cold tolerance by interacting with a JAZ protein and suppressing β-amylase expression.Crossref | GoogleScholarGoogle Scholar | 28062835PubMed |
Mackill DJ, Lei XM (1997) Genetic variation for traits related to temperate adaptation of rice cultivars. Crop Science 37, 1340–1346.
| Genetic variation for traits related to temperate adaptation of rice cultivars.Crossref | GoogleScholarGoogle Scholar |
Nagano AJ, Sato Y, Mihara M, Antonio BA, Motoyama R, Itoh H, Nagamura Y, Izawa T (2012) Deciphering and prediction of transcriptome dynamics under fluctuating field conditions. Cell 151, 1358–1369.
| Deciphering and prediction of transcriptome dynamics under fluctuating field conditions.Crossref | GoogleScholarGoogle Scholar | 23217716PubMed |
Nagata K, Fukuta Y, Shimizu H, Yagi T, Terao T (2002) Quantitative trait loci for sink size and ripening traits in rice (Oryza sativa L.). Breeding Science 52, 259–273.
| Quantitative trait loci for sink size and ripening traits in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
Ning J, Li XH, Hicks LM, Xiong LZ (2010) A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiology 152, 876–890.
| A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice.Crossref | GoogleScholarGoogle Scholar | 20007444PubMed |
Ohsumi A, Furuhata M, Matsumura O (2012) Varietal differences in biomass production of rice early after transplanting at low temperatures. Plant Production Science 15, 32–39.
| Varietal differences in biomass production of rice early after transplanting at low temperatures.Crossref | GoogleScholarGoogle Scholar |
Ohyanagi H, Tanaka T, Sakai H, Shigemoto Y, Yamaguchi K, Habara T, Fujii Y, Antonio BA, Nagamura Y, Imanishi T, Ikeo K, Itoh T, Gojobori T, Sasaki T (2006) The Rice Annotation Project Database (RAP-DB): hub for Oryza sativa ssp. japonica genome information. Nucleic Acids Research 34, D741–D744.
| The Rice Annotation Project Database (RAP-DB): hub for Oryza sativa ssp. japonica genome information.Crossref | GoogleScholarGoogle Scholar | 16381971PubMed |
Onaga G, Wydra KD, Koopmann B, Sere Y, von Tiedemann A (2017) Elevated temperature increases in planta expression levels of virulence related genes in Magnaporthe oryzae and compromises resistance in Oryza sativa cv. Nipponbare. Functional Plant Biology 44, 358–371.
| Elevated temperature increases in planta expression levels of virulence related genes in Magnaporthe oryzae and compromises resistance in Oryza sativa cv. Nipponbare.Crossref | GoogleScholarGoogle Scholar | 32480570PubMed |
Pradhan SK, Pandit E, Nayak DK, Behera L, Mohapatra T (2019) Genes, pathways and transcription factors involved in seedling stage chilling stress tolerance in indica rice through RNA-Seq analysis. BMC Plant Biology 19, 352
| Genes, pathways and transcription factors involved in seedling stage chilling stress tolerance in indica rice through RNA-Seq analysis.Crossref | GoogleScholarGoogle Scholar | 31412781PubMed |
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; Available from: https://www.R-project.org/.
Shen CX, Li D, He RH, Fang Z, Xia YM, Gao J, Shen H, Cao ML (2014) Comparative transcriptome analysis of RNA-seq data for cold-tolerant and cold-sensitive rice genotypes under cold stress. Journal of Plant Biology 57, 337–348.
| Comparative transcriptome analysis of RNA-seq data for cold-tolerant and cold-sensitive rice genotypes under cold stress.Crossref | GoogleScholarGoogle Scholar |
Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction. Physiologia Plantarum 126, 45–51.
| Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction.Crossref | GoogleScholarGoogle Scholar |
Takai T, Kondo M, Yano M, Yamamoto T (2010) A quantitative trait locus for chlorophyll content and its association with leaf photosynthesis in rice. Rice (New York, N.Y.) 3, 172–180.
| A quantitative trait locus for chlorophyll content and its association with leaf photosynthesis in rice.Crossref | GoogleScholarGoogle Scholar |
Takenaka Y, Nakano S, Tamoi M, Sakuda S, Fukamizo T (2009) Chitinase gene expression in response to environmental stresses in Arabidopsis thaliana: chitinase inhibitor allosamidin enhances stress tolerance. Bioscience, Biotechnology, and Biochemistry 73, 1066–1071.
| Chitinase gene expression in response to environmental stresses in Arabidopsis thaliana: chitinase inhibitor allosamidin enhances stress tolerance.Crossref | GoogleScholarGoogle Scholar | 19420714PubMed |
Terao T, Nagata K, Morino K, Hirose T (2010) A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice. Theoretical and Applied Genetics 120, 875–893.
| A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice.Crossref | GoogleScholarGoogle Scholar | 20151298PubMed |
Tibshirani R (1996) Regression shrinkage and selection via the Lasso. Journal of the Royal Statistical Society. Series B. Methodological 58, 267–288.
| Regression shrinkage and selection via the Lasso.Crossref | GoogleScholarGoogle Scholar |
Wang J, Jiang J, Oard JH (2000) Structure, expression and promoter activity of two polyubiquitin genes from rice (Oryza sativa L.). Plant Science 156, 201–211.
| Structure, expression and promoter activity of two polyubiquitin genes from rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 10936527PubMed |
Yamori W, Sakata N, Suzuki Y, Shikanai T, Makino A (2011) Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. The Plant Journal 68, 966–976.
| Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice.Crossref | GoogleScholarGoogle Scholar | 21848656PubMed |
Ye H, Du H, Tang N, Li X, Xiong L (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Molecular Biology 71, 291–305.
| Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice.Crossref | GoogleScholarGoogle Scholar | 19618278PubMed |
Yeh S, Moffatt BA, Griffith M, Xiong F, Yang DSC, Wiseman SB, Sarhan F, Danyluk J, Xue YQ, Hew CL, Doherty-Kirby A, Lajoie G (2000) Chitinase genes responsive to cold encode antifreeze proteins in winter cereals. Plant Physiology 124, 1251–1264.
| Chitinase genes responsive to cold encode antifreeze proteins in winter cereals.Crossref | GoogleScholarGoogle Scholar | 11080301PubMed |
Yogendra KN, Kushalappa AC (2016) Integrated transcriptomics and metabolomics reveal induction of hierarchies of resistance genes in potato against late blight. Functional Plant Biology 43, 766–782.
| Integrated transcriptomics and metabolomics reveal induction of hierarchies of resistance genes in potato against late blight.Crossref | GoogleScholarGoogle Scholar | 32480502PubMed |
Yoshida R, Kanno A, Sato T, Kameya T (1996) Cool-temperature-induced chlorosis in rice plants. 1. Relationship between the induction and a disturbance of etioplast development. Plant Physiology 110, 997–1005.
| Cool-temperature-induced chlorosis in rice plants. 1. Relationship between the induction and a disturbance of etioplast development.Crossref | GoogleScholarGoogle Scholar | 8819872PubMed |
You J, Chan ZL (2015) ROS regulation during abiotic stress responses in crop plants. Frontiers in Plant Science 6, 1092
| ROS regulation during abiotic stress responses in crop plants.Crossref | GoogleScholarGoogle Scholar | 26697045PubMed |
Zhang SH, Zheng JS, Liu B, Peng SB, Leung H, Zhao JL, Wang XF, Yang TF, Huang ZH (2014) Identification of QTLs for cold tolerance at seedling stage in rice (Oryza sativa L.) using two distinct methods of cold treatment. Euphytica 195, 95–104.
| Identification of QTLs for cold tolerance at seedling stage in rice (Oryza sativa L.) using two distinct methods of cold treatment.Crossref | GoogleScholarGoogle Scholar |
Zhang J, Luo W, Zhao Y, Xu Y, Song S, Chong K (2016) Comparative metabolomic analysis reveals a reactive oxygen species-dominated dynamic model underlying chilling environment adaptation and tolerance in rice. New Phytologist 211, 1295–1310.
| Comparative metabolomic analysis reveals a reactive oxygen species-dominated dynamic model underlying chilling environment adaptation and tolerance in rice.Crossref | GoogleScholarGoogle Scholar |
