Skip to main content
SpringerLink
Log in

Deep RNAseq indicates protective mechanisms of cold-tolerant indica rice plants during early vegetative stage

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Cold-tolerance in rice may be related to increased cellulose deposition in the cell wall, membrane fatty acids unsaturation and differential expression of several newly identified genes.

Abstract

Low temperature exposure during early vegetative stages limits rice plant’s growth and development. Most genes previously related to cold tolerance in rice are from the japonica subspecies. To help clarify the mechanisms that regulate cold tolerance in young indica rice plants, comparative transcriptome analysis of 6 h cold-treated (10 °C) leaves from two genotypes, cold-tolerant (CT) and cold-sensitive (CS), was performed. Differentially expressed genes were identified: 831 and 357 sequences more expressed in the tolerant and in the sensitive genotype, respectively. The genes with higher expression in the CT genotype were used in systems biology analyses to identify protein–protein interaction (PPI) networks and nodes (proteins) that are hubs and bottlenecks in the PPI. From the genes more expressed in the tolerant plants, 60% were reported as affected by cold in previous transcriptome experiments and 27% are located within QTLs related to cold tolerance during the vegetative stage. Novel cold-responsive genes were identified. Quantitative RT-PCR confirmed the high-quality of RNAseq libraries. Several genes related to cell wall assembly or reinforcement are cold-induced or constitutively highly expressed in the tolerant genotype. Cold-tolerant plants have increased cellulose deposition under cold. Genes related to lipid metabolism are more expressed in the tolerant genotype, which has higher membrane fatty acids unsaturation, with increasing levels of linoleic acid under cold. The CT genotype seems to have higher photosynthetic efficiency and antioxidant capacity, as well as more effective ethylene, Ca2+ and hormone signaling than the CS. These genes could be useful in future biotechnological approaches aiming to increase cold tolerance in rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aalto MK, Helenius E, Kariola T, Pennanen V, Heino P, Hõrak H, Puzõrjova I, Kollist H, Palva ET (2012) ERD15—an attenuator of plant ABA responses and stomatal aperture. Plant Sci 182:19–28

    Article  CAS  PubMed  Google Scholar 

  • Abuqamar S, Ajeb S, Sham A, Enan MR, Iratni R (2013) A mutation in the expansin-like A2 gene enhances resistance to necrotrophic fungi and hypersensitivity to abiotic stress in Arabidopsis thaliana. Mol Plant Pathol 14:813–827

    Article  CAS  PubMed  Google Scholar 

  • Adamski JM, Cargnelutti D, Sperotto RA, Terra TF, Rosa LMG, Cruz RP, Fett JP (2016) Identification and physiological characterization of two sister lines of indica rice (Oryza sativa L.) with contrasting levels of cold tolerance. Can J Plant Sci 96:197–214

    Article  CAS  Google Scholar 

  • Aguan K, Sugawara K, Susuki N, Kusano T (1991) Isolation of genes for low-temperature-induced proteins in rice by a simple subtractive method. Plant Cell Physiol 32:1285–1289

    CAS  Google Scholar 

  • Amaral MN, Arge LWP, Benitez LC, Danielowski R, Silveira SFS, Farias DR, Oliveira AC, Maia LC, Braga EJB (2016) Comparative transcriptomics of rice plants under cold, iron, and salt stresses. Funct Integr Genomics 16:567–579

    Article  PubMed  CAS  Google Scholar 

  • Andaya VC, McKill DJ (2003) Mapping of QTL associated with cold tolerance during the vegetative stage in rice. J Exp Bot 54:2579–2585

    Article  CAS  PubMed  Google Scholar 

  • Andaya VC, Tai TH (2006) Fine mapping of the qCTS12 locus, a major QTL for seedling cold tolerance in rice. Theor Appl Genet 113:467–475

    Article  CAS  PubMed  Google Scholar 

  • Assenov Y, Ramírez F, Schelhorn S-E, Lengauer T, Albrecht M (2008) Computing topological parameters of biological networks. Bioinformatics 24(2):282–284

    Article  CAS  PubMed  Google Scholar 

  • Bader GD, Hogue CW (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinform 4:2

    Article  Google Scholar 

  • Barrett T, Wilhite SE, Ledoux P et al (2013) NCBI GEO: archive for functional genomics data sets—update. Nucleic Acids Res 41(Database issue):D991–D995. https://doi.org/10.1093/nar/gks1193

    Google Scholar 

  • Bevilacqua CB, Basu S, Pereira A, Tseng TM, Zimmer PD, Burgos NR (2015) Analysis of stress-responsive gene expression in cultivated and weedy rice differing in cold stress tolerance. PLoS One 10:e0132100

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bligh EC, Dyer WJ (1959) A rapid method of total lipid. Extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Bonnecarrère V, Borsani O, Díaz P, Capdevielle F, Blanco P, Monza J (2011) Response to photoxidative stress induced by cold in japonica rice is genotype dependent. Plant Sci 180:726–732

    Article  PubMed  CAS  Google Scholar 

  • Breton G, Danyluk J, Charron J, Sarhan F (2003) Expression profiling and bioinformatic analyses of a novel stress-regulated multispanning transmembrane protein family from cereals and Arabidopsis. Plant Physiol 32:64–74

    Article  CAS  Google Scholar 

  • Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, Reforgiato-Recupero G, Martin C (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 3:1242–1255

    Article  CAS  Google Scholar 

  • Chandran AKN, Jeong HY, Jung K-H, Lee C (2016) Development of functional modules based on co-expression patterns for cell-wall biosynthesis related genes in rice. J Plant Biol 59:1–15

    Article  CAS  Google Scholar 

  • Chawade A, Lindlöf A, Olsson B, Olsson O (2013) Global expression profiling of low temperature induced genes in the chilling tolerant japonica rice Jumli Marshi. PLoS One 8:e81729

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen NA, Xu Y, Wang X, Du C, Du J, Yuan M, Xu Z, Chong K (2011) OsRAN2, essential for mitosis, enhances cold tolerance in rice by promoting export of intranuclear tubulin and maintaining cell division under cold stress. Plant Cell Environ 34:52–64

    Article  CAS  PubMed  Google Scholar 

  • Cheng C, Yun KY, Ressom HW, Mohanty B, Bajic VB, Jia Y, Yun SJ, de los Reyes BG (2007) An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. BMC Genom 8:175

    Article  CAS  Google Scholar 

  • Cheng YW, Feng AQ, Zhang ZB, Zhang YZ, Han JM (2014) The phylogenetic analysis and identification of a novel remorin member from rice (Oryza sativa L) by proteomics under salt stress. Adv Mat Res 1073–1076:229–232

    Google Scholar 

  • Chinnusamy V, Zhu JK, Sunkar R (2010) Gene regulation during cold stress acclimation in plants. Methods Mol Biol 639:39–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signaling in plant responses to abiotic stress. J Exp Biol 217:67–75

    Article  CAS  PubMed  Google Scholar 

  • Conesa A, Götz A (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genom 2008:619832

  • Copetti D, Zhang J, El Baidouri M, Gao D, Wang J, Barghini E, Cossu RM, Angelova A, Maldonado LCE, Roffler S, Ohyanagi H, Wicker T, Fan C, Zuccolo A, Chen M, de Oliveira AC, Han B, Henry R, Hsing Y-I, Kurata N, Wang W, Jackson SA, Panaud O, Wing RA (2015) RiTE database: a resource database for genus-wide rice genomics and evolutionary biology. BMC Genom 16:538

    Article  CAS  Google Scholar 

  • Cruz RP, Milach SCK (2004) Cold tolerance at the germination stage of rice: methods of evaluation and characterization of genotypes. Sci Agric 61:1–8

    Article  Google Scholar 

  • Cruz RP, Golombieski JI, Bazana MT, Cabreira C, Silveira TF, da Silva LP (2010) Alterations in fatty acid composition due to cold exposure at the vegetative stage in rice. Braz J Plant Physiol 22:199–207

  • Cruz RP, Sperotto RA, Cargnelutti D, Adamski JM, Terra TF, Fett JP (2013) Avoiding damage and achieving cold tolerance in rice plants. Food Energy Secur 2:96–119

    Article  Google Scholar 

  • Dametto A, Sperotto RA, Adamski JM, Blasi EA, Cargnelutti D, de Oliveira LF, Ricachenevsky FK, Fregonezi JN, Mariath JE, da Cruz RP, Margis R, Fett JP (2015) Cold tolerance in rice germinating seeds revealed by deep RNAseq analysis of contrasting indica genotypes. Plant Sci 238:1–12

    Article  CAS  PubMed  Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought, high-salt- and cold-responsive gene expression. Plant J 33:751–763

    Article  CAS  PubMed  Google Scholar 

  • El Baidouri M, Panaud O (2013) Comparative genomic paleontology across plant kingdom reveals the dynamics of TE-driven genome evolution. Genome Biol Evol 5:954–965

    Article  PubMed  PubMed Central  Google Scholar 

  • Endler A, Kesten C, Schneider R, Zhang Y, Ivakov A, Froehlich A, Funke N, Persson S (2015) A mechanism for sustained cellulose synthesis during salt stress. Cell 162:1353–1364

    Article  CAS  PubMed  Google Scholar 

  • Endler A, Schneider R, Kesten C, Lampugnani ER, Persson S (2016) The cellulose synthase companion proteins act non-redundantly with CELLULOSE SYNTHASE INTERACTING1/POM2 and CELLULOSE SYNTHASE 6. Plant Signal Behav 11(4):e1135281

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fang H, Meng Q, Xu J, Tang H, Tang S, Zhang H, Huang J (2015) Knock-down of stress inducible OsSRFP1 encoding an E3 ubiquitin ligase with transcriptional activation activity confers abiotic stress tolerance through enhancing antioxidant protection in rice. Plant Mol Biol 87:441–458

    Article  CAS  PubMed  Google Scholar 

  • FinattoT, De Oliveira AC, Chaparro C, Da Maia LC, Farias DR, Woyann LG, etal (2015). Abiotic stress and genome dynamics: specific genes and transposable elements response to iron excess in rice. Rice 8:1. https://doi.org/10.1186/s12284-015-0045-6

    Article  Google Scholar 

  • Frenette Charron JB, Breton G, Badawi M, Sarhan F (2002) Molecular and structural analyses of a novel temperature stress-induced lipocalin from wheat and Arabidopsis. FEBS Lett 517:129–132

    Article  CAS  PubMed  Google Scholar 

  • Gothandam KM, Nalini E, Karthikeyan S, Shin JS (2010) OsPRP3, a flower specific proline-rich protein of rice, determines extracellular matrix structure of floral organs and its overexpression confers cold-tolerance. Plant Mol Biol 72:125–135

    Article  CAS  PubMed  Google Scholar 

  • Guo-Li W, Zhen-Fei G (2005) Effects of chilling stress on photosynthetic rate and chlorophyll fluorescence parameter in seedlings of two rice cultivars differing in cold tolerance. Rice Sci 12:187–191

    Google Scholar 

  • Hartman L, Lago BCA (1973) Rapid preparation of fatty, methyl esters from lipids. Lab Pract 22:457–477

    Google Scholar 

  • Hatakeyama S, Yada M, Matsumoto M, Ishida N, Nakayama KI (2001) U box proteins as a new family of ubiquitin-protein ligases. J Biol Chem 276(35):33111–33120

    Article  CAS  PubMed  Google Scholar 

  • He ZH, Dong HT, Dong JX, Li DB, Ronald PC (2000) The rice Rim2 transcript accumulates in response to Magnaporthe grisea and its predicted protein product shares similarity with TNP2- like proteins encoded by CACTA transposons. Mol Gen Genet 264:2–10

    Article  CAS  PubMed  Google Scholar 

  • Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang J, Sun S, Xu D, Lan H, Sun H, Wang Z, Bao Y, Wang J, Tang H, Zhang H (2012) A TFIIIA-type zinc finger protein confers multiple abiotic stress tolerances in transgenic rice (Oryza sativa L.). Plant Mol Biol 80:337–350

    Article  CAS  PubMed  Google Scholar 

  • Huang F, Lian L, He W, Zhu Y, Cai Q, Xie H, Zhang J (2014a) Genome-wide profiling of changes in gene expression in response to infection of the japonica rice variety Yunyin by Magnaporthe oryzae. Mol Breed 34:1965–1974

    Article  CAS  Google Scholar 

  • Huang L, Zhang F, Zhang F, Wang W, Zhou Y, Fu B, Li Z (2014b) Comparative transcriptome sequencing of tolerant rice introgression line and its parents in response to drought stress. BMC Genom 15:1026

    Article  CAS  Google Scholar 

  • Huang L, Hong Y, Zhang H, Li D, Song F (2016) Rice NAC transcription factor ONAC095 plays opposite roles in drought and cold stress tolerance. BMC Plant Biol 16:203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Iba K (2002) Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu Rev Plant Biol 53:225–245

    Article  CAS  PubMed  Google Scholar 

  • Inagaki Y-S, Ethrerington G, Geisler K, Field B, Dokarry M, Ikeda K, Mutsukado Y, Dicks J, Osbourn A (2011) Investigation of the potential for triterpene synthesis in rice through genome mining and metabolic engineering. New Phytol 191:432–448

    Article  CAS  PubMed  Google Scholar 

  • IRGSP-International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  CAS  Google Scholar 

  • Ishiguro S, Ogasawara K, Fujino K, Sato Y, Kishima Y (2014) Low temperature-responsive changes in the anther transcriptome’s repeat sequences are indicative of stress sensitivity and pollen sterility in rice strains. Plant Physiol 164:671–682. https://doi.org/10.1104/pp.113.230656

    Article  CAS  PubMed  Google Scholar 

  • Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153

    Article  CAS  PubMed  Google Scholar 

  • Jami SK, Clark GB, Ayele BT, Roux SJ, Kirti PB (2012) Identification and characterization of annexin gene family in rice. Plant Cell Rep 31:813–825

    Article  CAS  PubMed  Google Scholar 

  • Jarsch IK, Ott T (2011) Perspectives on remorin proteins, membrane rafts, and their role during plant-microbe interactions. Mol Plant Microbe Interact 24:7–12

    Article  CAS  PubMed  Google Scholar 

  • Jiang L, Xun M, Wang J, Wan J (2008) QTL analysis of cold tolerance at seedling stage in rice (Oryza sativa L.) using recombination inbred lines. J Cereal Sci 48:173–179

    Article  CAS  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kargiotidou A, Deli D, Galanopolou D, Tsaftaris A, Farmaki T (2008) Low temperature and light regulate delta 12 fatty acid desaturases (FAD2) at a transcriptional level in cotton (Gossypium hirsutum). J Exp Bot 59:2043–2056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim SJ, Lee SC, Hong SK, An K, An G, Kim SR (2009) Ectopic expression of a cold-responsive OsAsr1 cDNA gives enhanced cold tolerance in transgenic rice plants. Mol Cells 27:449–458

    Article  CAS  PubMed  Google Scholar 

  • Kim SM, Suh JP, Lee CK, Lee JH, Kim YG, Jena KK (2014) QTL mapping and development of candidate gene-derived DNA markers associated with seedling cold tolerance in rice (Oryza sativa L.). Mol Genet Genom 289:333–343

    Article  CAS  Google Scholar 

  • Konopka-Postupolska D, Clark G, Hofmann A (2011) Structure, function and membrane interactions of plant annexins: an update. Plant Sci 181:230–241

    Article  CAS  PubMed  Google Scholar 

  • Koseki M, Kitazawa N, Yonebayashi S, Maehara Y, Wang ZX, Minobe Y (2010) Identification and fine mapping of a major quantitative trait locus originating from wild rice, controlling cold tolerance at the seedling stage. Mol Genet Genom 284:45–54

    Article  CAS  Google Scholar 

  • Kumari S, Sabharwal VP, Kushwaha HR, Sopory SK, Singla-Pareek SL, Pareek A (2009) Transcriptome map for seedling stage specific salinity stress response indicates a specific set of genes as candidate for saline tolerance in Oryza sativa L. Funct Integr Genom 9:109–123

    Article  CAS  Google Scholar 

  • Kunze M, Pracharoenwattana I, Smith SM, Hartig A (2006) A central role for the peroxisomal membrane in glyoxylate cycle function. Biochim Biophys Acta 1763:1441–1452

    Article  CAS  PubMed  Google Scholar 

  • Lee SC, Huh KW, An K, An G, Kim SR (2004a) Ectopic expression of a cold-inducible transcription factor, CBF1/DREB1b, in transgenic rice (Oryza sativa L.). Mol Cells 18:107–114

    CAS  PubMed  Google Scholar 

  • Lee S, Lee EJ, Yang EJ, Lee JE, Park AR, Song WH, Park OK (2004b) Proteomic identification of annexins, calcium-dependent membrane binding proteins that mediate osmotic stress and abscisic acid signal transduction in Arabidopsis. Plant Cell 16:1378–1391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SC, Lee MY, Kim SJ, Jun SH, An G, Kim SR (2005) Characterization of an abiotic stress-inducible dehydrin gene, OsDhn1, in rice (Oryza sativa L.). Mol Cells 19:212–218

    CAS  PubMed  Google Scholar 

  • Lee J, Lee W, Kwon SW (2015) A quantitative shotgun proteomics analysis of germinated rice embryos and coleoptiles under low-temperature conditions. Proteome Sci 13:27

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li TG, Visperas RM, Vergara BS (1981) Correlation of cold tolerance at different growth stages in rice. Acta Bot Sin 23:203–207

    Google Scholar 

  • Li Y, Qian Q, Zhou Y, Yan M, Sun L, Zhang M, Fu Z, Wang Y, Han B, Pang X, Chen M, Li J (2003) BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15:2020–2031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindlöf A, Chawade A, Sikora P, Olsson O (2015) Comparative transcriptomics of Sijung and Jumli Marshi rice during early chilling stress imply multiple protective mechanisms. PLoS One 10:e0125385

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu CW, Hsu YK, Cheng YH, Yen HC, Wu YP, Wang CS, Lai CC (2012) Proteomic analysis of salt-responsive ubiquitin-related proteins in rice roots. Rapid Commun Mass Spectrom 26:1649–1660

    Article  CAS  PubMed  Google Scholar 

  • Lou Q, Chen L, Sun Z, Xing Y, Li J, Xu X, Mei H, Luo L (2007) A major QTL associated with cold tolerance at seedling stage in rice (Oryza sativa L.). Euphytica 158:87–94

    Article  CAS  Google Scholar 

  • Lourenço T, Sapeta H, Figueiredo DD, Rodrigues M, Cordeiro A, Abreu IA, Saibo NJ, Oliveira MM (2013) Isolation and characterization of rice (Oryza sativa L.) E3-ubiquitin ligase OsHOS1 gene in the modulation of cold stress response. Plant Mol Biol 83:351–363

    Article  PubMed  CAS  Google Scholar 

  • Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D, Xiao J, Guo X, Xu S, Niu Y, Jin J, Zhang H, Xu X, Li L, Wang W, Qian Q, Ge S, Chong K (2015) COLD1 confers chilling tolerance in rice. Cell 160:1209–1221

    Article  CAS  PubMed  Google Scholar 

  • Mackill DJ, Lei X (1997) Genetic variation for traits related to temperate adaptation of rice cultivars. Crop Sci 37:1340–1346

    Article  Google Scholar 

  • Makarevitch I, Waters AJ, West PT, Stitzer M, Hirsch CN et al (2015) Transposable Elements Contribute to Activation of Maize Genes in Response to Abiotic Stress. PLoS Genet 11(1):e1004915. https://doi.org/10.1371/journal.pgen.1004915

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mertz LM, Henning FA, Soares RC, Baldiga RF, Peske FB, Moraes DM (2009) Physiological changes in rice seeds exposed to cold in the germination phase. Rev Bras Sem 31:254–262

    Google Scholar 

  • Mishra M, Kanwar P, Singh A, Pandey A, Kapoor S, Pandey GK (2003) Plant Omics: genome-wide analysis of ABA Repressor1 (ABR1) related genes in rice during abiotic stress and development. OMICS 17(8): 439–450

    Article  CAS  PubMed  Google Scholar 

  • Mittal D, Madhyastha DA, Grover A (2012) Genome-wide transcriptional profiles during temperature and oxidative stress reveal coordinated expression patterns and overlapping regulons in rice. PLoS One 7:e40899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizutani M (2012) Impacts of diversification of cytochrome P450 on plant metabolism. Biol Pharm Bull 35:824–832

    Article  CAS  PubMed  Google Scholar 

  • Mori M, Onishi K, Tokizono Y, Shinada H, Yushimura T, Numao Y et al (2011) Detection of a novel quantitative trait loci for cold tolerance at the booting stage derived from a tropical japonica rice variety Silewah. Breed Sci 61:61–68

    Article  Google Scholar 

  • Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713

    Article  CAS  Google Scholar 

  • Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, Okumoto Y, Tanisaka T, Wessler SR (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630

    Article  CAS  PubMed  Google Scholar 

  • Negi P, Rai AN, Suprasanna P (2016) Moving through the stressed genome: emerging regulatory roles for transposons in plant stress response. Front Plant Sci 7:1448

    PubMed  PubMed Central  Google Scholar 

  • Neumann P, Yan H, Jiang J (2007) The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference. Genetics 176:749–761. https://doi.org/10.1534/genetics.107.071902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nie D-M, Ouyang Y-D, Wang X, Zhou W, Hu C-G, Yao J (2013) Genome-wide analysis of endosperm-specific genes in rice. Gene 530:236–247

    Article  CAS  PubMed  Google Scholar 

  • O’Brien JA, Benková E (2013) Cytokinin cross-talking during biotic and abiotic stress responses. Front Plant Sci 4:451

    Article  PubMed  PubMed Central  Google Scholar 

  • Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-S P (2013) Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J Exp Bot 64:445–458

    Article  CAS  PubMed  Google Scholar 

  • Pan Y, Zhang H, Zhang D, Li J, Xiong H, Yu J et al (2015) Genetic analysis of cold tolerance at the germination and booting stages in rice by association mapping. PLoS One 10:e0120590

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raffaele S, Mongrand S, Gamas P, Niebel A, Ott T (2007) Genome-wide annotation of remorins, a plant-specific protein family: evolutionary and functional perspectives. Plant Physiol 145:593–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman A (2013) Auxin: a regulator of cold stress response. Physiol Plant 147:28–35

    Article  CAS  PubMed  Google Scholar 

  • Ranawake AL, Manangkil OE, Yoshida S, Ishii T, Mori N, Nakamura C (2014) Mapping QTLs for cold tolerance at germination and the early seedling stage in rice (Oryza sativa L.). Biotechnol Biotechnol Equip 28:989–998

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) EdgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  CAS  PubMed  Google Scholar 

  • Román A, Andreu V, Hernández ML, Lagunas B, Picorel R, Martínez-Rivas JM, Alfonso M (2012) Contribution of the different omega-3 fatty acid desaturase genes to the cold response in soybean. J Exp Bot 63:4973–4982

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Routaboul JM, Fischer SF, Browse J (2000) Trienoic fatty acids are required to maintain chloroplast function at low temperatures. Plant Physiol 124:1697–1705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327

    Article  CAS  PubMed  Google Scholar 

  • Saito KSY, Kuroki M, Sato Y (2010) Map-based cloning of the rice cold tolerance gene Ctb1. Plant Sci 179:97–102

    Article  CAS  Google Scholar 

  • Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, Wakimoto H, Yang CC, Iwamoto M, Abe T, Yamada Y, Muto A, Inokuchi H, Ikemura T, Matsumoto T, Sasaki T, Itoh T (2013) Rice annotation project database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54(2):e6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genom 12:30–43

    Article  CAS  Google Scholar 

  • Sato Y, Masuta Y, Saito K, Murayama S, Ozawa K (2011) Enhanced chilling tolerance at the booting stage in rice by transgenic overexpression of the ascorbate peroxidase gene, OsAPXa. Plant Cell Rep 30:399–406

    Article  CAS  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    Article  CAS  PubMed  Google Scholar 

  • Schuler MA, Werck-Reichhart D (2003) Functional Genomics of P450s. Annu Rev Plant Biol 54:629–667

    Article  CAS  PubMed  Google Scholar 

  • Shakiba E, Edwards JD, Jodari F, Duke SE, Baldo AM, Korniliev P et al. (2017) Genetic architecture of cold tolerance in rice (Oryza sativa) determined through high resolution genome-wide analysis. PLoS One 12(3): e0172133. https://doi.org/10.1371/journal.pone.0172133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi J, Cao Y, Fan X, Li M, Wang Y, Ming F (2012) A rice microsomal delta-12 fatty acid desaturase can enhance resistance to cold stress in yeast and Oryza sativa. Mol Breed 29:743–757

    Article  CAS  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590

    Article  CAS  PubMed  Google Scholar 

  • Song X, Cao X (2017) Transposon-mediated epigenetic regulation contributes to phenotypic diversity and environmental adaptaion in rice. Curr Opin Plant Biol 36:111–118

    Article  CAS  PubMed  Google Scholar 

  • Songyikhangsuthor K, Guo Z, Wang N, Zhu X, Xie W, Mou T, Xiong L (2014) Natural variation in the sequence of SNAC1 and its expression level polymorphism in rice germplasms under drought stress. J Genet Genom 41:609–612

    Article  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Chlorophyll a fluorescence: a signature of photosynthesis, analysis of the chlorophyll a fluorescence transient, vol 14. Springer, Dordrecht, pp 321–362 (Chapter 12)

    Book  Google Scholar 

  • Su CF, Wang YC, Hsieh TH, Lu CA, Tseng TH, Yu SM (2010) A novel MYBS3-dependent pathway confers cold tolerance in rice. Plant Physiol 153:145–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C (2015) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:447–452

    Article  CAS  Google Scholar 

  • Takahashi N (1984) Differentiation of ecotypes in Oryza sativa. In: Takahashi N, Tsunoda S (eds) Biology of rice. Japan Science Society, Tokyo, pp 31–67

    Chapter  Google Scholar 

  • Tang W, Page M (2013) Transcription factor AtbZIP60 regulates expression of Ca2+-dependent protein kinase genes in transgenic cells. Mol Biol Rep 40:2723–2732

    Article  CAS  PubMed  Google Scholar 

  • Tao Z, Kou Y, Liu H, Li X, Xiao J, Wang S (2011) OsWRKY45 alleles play different roles in abscisic acid signaling and salt stress tolerance but similar roles in drought and cold tolerance in rice. J Exp Bot 62:4863–4874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian Y, Zhang H, Pan X, Chen X, Zhang Z, Lu X et al (2011) Overexpression of ethylene response factor TERF2 confers cold tolerance in rice seedlings. Transg Res 20:857–866

    Article  CAS  Google Scholar 

  • Tittel-Elmer M, Bucher E, Broger L, Mathieu O, Paszkowski J, Vaillant I et al (2010) Stress-induced activation of heterochromatic transcription. PLoS Genet 6:e1001175. https://doi.org/10.1371/journal.pgen.1001175

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tovuu A, Zulfugarov I, Wu G, Kang IS, Kim C, Moon BY, An G, Lee C-H (2016) Rice mutants deficient in ω-3 fatty acid desaturase (FAD8) fail to acclimate to cold temperatures. Plant Phys Biochem 109:525–535

    Article  CAS  Google Scholar 

  • Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M (2009) A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, maize. Plant Cell Environ 32:1211–1229

    Article  PubMed  Google Scholar 

  • Valitova JN, Sulkarnayeva AG, Minibayeva FV (2016) Plant Sterols: diversity, biosynthesis, and physiological functions. Biochem (Moscow) 81:819–834

    Article  CAS  Google Scholar 

  • Vij S, Giri J, Dansana PK, Kapoor S, Tyagi AK (2008) The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress. Mol Plant 1:732–750

    Article  CAS  PubMed  Google Scholar 

  • Wang GD, Tian PF, Cheng Z-K, Wu ZK, Jiang G, Li JM, Li DB, He Q ZH (2003) Genomic characterization of Rim2 / Hipa elements reveals a CACTA-like transposon superfamily with unique features in the rice genome. Mol Gen Genom 270:234–242

    Article  CAS  Google Scholar 

  • Wang Q, Guan Y, Wu Y, Chen H, Chen F, Chu C (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602

    Article  CAS  PubMed  Google Scholar 

  • Wen JQ, Oono K, Imai R (2002) Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice. Plant Physiol 129:1880–1891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538

    Article  CAS  PubMed  Google Scholar 

  • Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotech J 8:749–771

    Article  CAS  Google Scholar 

  • Wu Y-S, Yang C-Y (2016) Physiological responses and expression profile of NADPH oxidase in rice (Oryza Sativa) seedlings under different levels of submergence. Rice 9:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie G, Kato H, Imai R (2012) Biochemical identification of the OsMKK6-OsMPK3 signaling pathway for chilling stress tolerance in rice. Biochem J 443:95–102

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi T, Nakayama K, Hayashi T, Yazaki J, Kishimoto N, Kikuchi S, Koike S (2004) cDNA microarray analysis of rice anther genes under chilling stress at the microsporogenesis stage revealed two genes with DNA transposon Castway in the 5′-flanking region. Biosci Biotechnol Biochem 68(6):1315–1323

    Article  CAS  PubMed  Google Scholar 

  • Yan YS, Chen XY, Yang K, Sun ZX, Fu YP, Zhang YM, Fang RX (2011) Overexpression of an F-box protein gene reduces abiotic stress tolerance and promotes root growth in rice. Mol Plant 4:190–197

    Article  CAS  PubMed  Google Scholar 

  • Yang YW, Chen HC, Jen WF, Liu LY, Chang MC (2015) Comparative transcriptome analysis of shoots and roots of TNG67 and TCN1 rice seedlings under cold stress and following subsequent recovery: insights into metabolic pathways, phytohormones, and transcription factors. PLoS One 10:e0131391

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 Mol Biol 71:291–305

    Article  CAS  PubMed  Google Scholar 

  • Yen SK, Chung MC, Chen PC, Yen HE (2001) Environmental and developmental regulation of the wound-induced cell wall protein WI12 in the halophyte ice plant. Plant Physiol 127:517–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeller G, Henz SR, Widmer CK, Sachsenberg T, Rätsch G, Weigel D et al (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58:1068–1082. https://doi.org/10.1111/j.1365-313X.2009.03835.x

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZH, Qu XS, Wan S, Chen LH, Zhu YG (2005) Comparison of QTL controlling seedling vigour under different temperature conditions using recombinant inbred lines in rice (Oryza sativa). Ann Bot 95:423–429

  • Zhang T, Zhao X, Wang W, Pan Y, Huang L, Liu X et al (2012a) Comparative transcriptome profiling of chilling stress responsiveness in two contrasting rice genotypes. PLoS One 7:e43274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Huang L, Wang W, Zhao X, Zhu L, Fu B, Li Z (2012b) Genome-wide gene expression profiling of introgressed indica rice alleles associated with seedling cold tolerance improvement in a japonica rice background. BMC Genom 13:461

    Article  CAS  Google Scholar 

  • Zhang Q, Jiang N, Wang GL, Hong Y, Wang Z (2013) Advances in understanding cold sensing and the cold-responsive network in rice. Adv Crop Sci Technol 1:1

    Google 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 Phytol 211:1295–1310. https://doi.org/10.1111/nph.14011

    Article  CAS  PubMed  Google Scholar 

  • Zheng M, Wang Y, Liu K, Shu H, Zhou Z (2012) Protein expression changes during cotton fiber elongation in response to low temperature stress. J Plant Physiol 169:399–409

    Article  CAS  PubMed  Google Scholar 

  • Zheng W, Ma L, Zhao J, Li Z, Sun F, Lu X (2013) Comparative transcriptome analysis of two rice varieties in response to rice stripe virus and small brown planthoppers during early interaction. PLoS One 8:e82126

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhiguo E, Zhang Y, Li T, Wang L, Zhao H (2015) Characterization of the ubiquitin-conjugating enzyme gene family in rice and evaluation of expression profiles under abiotic stresses and hormone treatments. PLoS One 10(4):e0122621. https://doi.org/10.1371/journal.pone.0122621

    Article  CAS  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Chen K, Mi X, Chen T, Ali J, Ye G et al (2015) Identification and fine mapping of a stably expressed QTL for cold tolerance at the booting stage using an interconnected breeding population in rice. PLoS One 10:e0145704

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Universidade do Vale do Taquari - UNIVATES and the Brazilian funding agencies FAPERGS (Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico). The authors thank IRGA (Instituto Rio-Grandense do Arroz) for providing the rice seeds, for access to its facilities and for technical support.

Author information

Author notes

    Authors and Affiliations

    1. Centro de Ciências Biológicas e da Saúde (CCBS), Programa de Pós-Graduação em Biotecnologia (PPGBiotec), Universidade do Vale do Taquari-UNIVATES, Lajeado, RS, Brazil

      Raul Antonio Sperotto

    2. Centro de Biotecnologia, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil

      Artur Teixeira de Araújo Junior, Ben-Hur Neves de Oliveira & Janette Palma Fett

    3. Departamento de Botânica, Instituto de Biociências, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil

      Janete Mariza Adamski, Rinaldo Pires dos Santos & Janette Palma Fett

    4. Departamento de Agronomia, Universidade Federal da Fronteira Sul (UFFS), Erechim, RS, Brazil

      Denise Cargnelutti

    5. Departamento de Biologia, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil

      Felipe Klein Ricachenevsky

    6. Departamento de Plantas de Lavoura, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil

      Renata Pereira da Cruz

    7. Departamento de Zootecnia, Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brazil

      Leila Picolli da Silva

    Authors
    1. Raul Antonio Sperotto
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Artur Teixeira de Araújo Junior
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Janete Mariza Adamski
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Denise Cargnelutti
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Felipe Klein Ricachenevsky
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Ben-Hur Neves de Oliveira
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Renata Pereira da Cruz
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Rinaldo Pires dos Santos
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Leila Picolli da Silva
      View author publications

      You can also search for this author in PubMed Google Scholar

    10. Janette Palma Fett
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Raul Antonio Sperotto or Janette Palma Fett.

    Ethics declarations

    Conflict of interest

    The authors declare that they have no conflict of interest.

    Additional information

    Communicated by Marcelo Menossi.

    Raul Antonio Sperotto, Artur Teixeira de Araújo Junior and Janete Mariza Adamski contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    299_2017_2234_MOESM1_ESM.jpg

    Fig. 1. Visual symptoms of rice plants from the cold-tolerant (CT) and cold-sensitive (CS) genotypes after 10 days under control (28 °C) or cold (10 °C) treatment, followed by 7 days of recovery at 28 °C. Bar in figure (A) indicates 7 cm. The experiment was performed twice with similar results (JPG 2062 KB)

    299_2017_2234_MOESM2_ESM.jpg

    Fig. 2. Analysis of genes expressed in leaves from two indica rice genotypes (cold-tolerant (CT) and cold-sensitive (CS)). (A) Scatter plot comparing the gene expression levels between the CT and the CS genotypes. (B) Genes identified by red dots have adjusted p-value lower than 0.000001 (calculated using EdgeR). FC: fold change; CPM: counts per million (JPG 2368 KB)

    Table 1. Gene-specific PCR primers used for RT-qPCR (DOC 42 KB)

    299_2017_2234_MOESM4_ESM.xlsx

    Table 2. Differentially expressed genes revealed by RNAseq in leaves of rice plants exposed to cold treatment (10 °C) for 6 h. First panel: genes with higher expression in the cold-tolerant genotype (IRGA 959-1-2-2F-4-1-4-A). Second panel: genes with higher expression in the cold-sensitive genotype (IRGA 959-1-2-2F-4-1-4-D-1-CA-1) (XLSX 296 KB)

    299_2017_2234_MOESM5_ESM.xlsx

    Table 3. Meta-analysis of cold-responsive genes. All genes considered differentially expressed in this work (with higher expression in the cold-tolerant or in the cold-sensitive genotypes after plant exposure to 10 °C for 6 h) were used in searches for matching genes in tables of differentially expressed genes (in rice plants under cold treatment) reported in previous large-scale research papers. Details from each experiment are provided in the third spreadsheet. In the first two spreadsheets, genes that were reported as cold-responsive in at least one of the previous works are shown in red letters. Results obtained with rice genotypes considered cold-tolerant are shaded in blue, while results from cold-sensitive genotypes are shaded in yellow. Results obtained with rice Nipponbare are not shaded, because there is controversy about its sensitivity to cold. In the fourth spreadsheet, gene locations were compared with locations of QTLs previously identified as related to cold tolerance in rice plants during the vegetative stage. Genes with corresponding locations (“hits”) are marked with X in the corresponding columns and are shown in blue letters (XLSX 376 KB)

    299_2017_2234_MOESM6_ESM.xlsx

    Table 4. Descriptions of genes/proteins present in the response interactome of the cold-tolerant indica rice plants. Nodes with differentially expressed genes (higher expression in the cold-tolerant than in the sensitive plants) revealed by RNAseq in leaves of rice plants exposed to cold treatment (10 °C) for 6 h have fold change (FC Tolerant/Sensitive) shown in column D. The description (Hit) and gene ontology of each node was obtained from the Rice Genome Annotation Project (RGAP) database. The data of node degree and betweeneess centrality were obtained with a plugin network analyzer in the Cytoscape software. The metabolism categories were determined using the KEGG database (XLSX 70 KB)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Sperotto, R.A., de Araújo Junior, A.T., Adamski, J.M. et al. Deep RNAseq indicates protective mechanisms of cold-tolerant indica rice plants during early vegetative stage. Plant Cell Rep 37, 347–375 (2018). https://doi.org/10.1007/s00299-017-2234-9

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00299-017-2234-9

    Keywords

    Search

    Navigation