Abstract
Main conclusion
Major metabolic pathways and genes affected by low-temperature treatment were identified and a thorough picture of the early transcriptional changes in sugar beet plantlets upon cold stress was given.
Sugar beet (Beta vulgaris L.) is an important source of sugar and bioethanol production in temperate areas worldwide. In these areas, plantlet survival and sucrose yield of mature plants can be seriously limited by low temperatures, especially when plantlets are exposed to freezing temperatures (below 0 °C) at the early developmental stages. This frequently occurs when the crop is sown in early spring or even in autumn (autumn sowing) to escape drought at maturity and pathogen outbreaks. The knowledge of molecular responses induced in plantlets early upon exposure to low temperature is necessary to understand mechanisms that allow the plant to survive and to identify reactions that can influence other late-appearing traits. In this work, a wide study of sugar beet transcriptome modulation after a short exposure to a cold stress, mimicking what is experienced in vivo by young plantlets when temperature drops in the early spring nights, was carried out by high-throughput sequencing of leaves and root RNAs (RNA-Seq). A significant picture of the earliest events of temperature sensing was achieved for the first time for sugar beet: the retrieval of a great amount of transcription factors and the intensity of modulation of a large number of genes involved in several metabolic pathways suggest a fast and deep rearrangement of sugar beet plantlets metabolism as early response to cold stress, with both similarities and specificities between the two organs.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- AF:
-
Antifreeze protein
- AP2/ERF:
-
Apetala2/ethylene responsive
- BR:
-
Brassinosteroid
- CBF/DREB:
-
C-repeat binding factor/dehydration responsive element- binding factor
- COR:
-
Cold responsive
- DE:
-
Differentially expressed
- FPKM:
-
Fragments per kilobase of exon per million fragments mapped
- FunCat:
-
Functional Catalogue
- GO:
-
Gene ontology
- PR:
-
Pathogenesis-related
- ROS:
-
Reactive oxygen species
- TF:
-
Transcription factor
References
Abou-Elwafa SF, Büttner B, Kopisch-Obuch FJ, Jung C, Müller AE (2012) Genetic identification of a novel bolting locus in Beta vulgaris which promotes annuality independently of the bolting gene B. Mol Breed 29:989–998
Agribusiness Handbook (2009) Sugar beet—white sugar. Food and Agriculture Organization of the United Nations (ed), Rome
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106. doi:10.1186/gb-2010-11-10-r106
Arisz SA, van Wijk R, Roels W, Zhu JK, Haring MA, Munnik T (2013) Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase. Front Plant Sci 4:1. doi:10.3389/fpls.2013.00001
Badawi M, Danyluk J, Boucho B, Houde M, Sahran F (2007) The CBF gene family in hexaploid wheat and its relationship to the phylogenetic complexity of cereal CBFs. Mol Genet Genomics 277:533–554
Badawi M, Reddy YV, Agharbaoui Z, Tominaga Y, Danyluk J, Sahran F, Houde M (2008) Structure and functional analysis of wheat ICE (Inducer of CBF Expression) genes. Plant Cell Physiol 49:1237–1249
Bellin D, Werber M, Theis T, Schulz B, Weisshaar B, Schneider K (2002) EST sequencing, annotation and macroarray transcriptome analysis identify preferentially root-expressed genes in sugar beet. Plant Biol 4:700–710
Biancardi E, Panella LW, Lewellen RT (2012) Beta maritima: the origin of beets. Springer, New York
Bilyeu KD, Cole JL, Laskey JG, Riekhof WR, Esparza TJ, Kramer MD, Morris RO (2001) Molecular and biochemical characterization of a cytokinin oxidase from maize. Plant Physiol 125:378–386
Cantrel C, Vazquez T, Puyaubert J, Rezé N, Lesch M, Kaiser WM, Dutilleul C, Guillas I, Zachowski A, Baudouin E (2011) Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytol 1:415–427
Casique-Arroyo G, Martinez-Gallardo N, González de la Vara L, Délano-Frier JP (2014) Betacyanin biosynthetic genes and enzymes are differentially induced by (a)biotic stress in Amaranthus hypochondriacus. PLoS ONE 9:e99012. doi:10.1371/journal.pone.0099012
Catusse J, Strub JM, Job C, van Dorsselaer A, Job D (2008) Proteome-wide characterization of sugarbeet seed vigor and its tissue specific expression. Proc Natl Acad Sci USA 105:10262–10267
Chen M, Markham JE, Cahoon EB (2012) Sphingolipid ∆8 unsaturation is important for glucosylceramide biosynthesis and low-temperature performance in Arabidopsis. Plant J 69:769–781
Chinnusamy V, Ohta M, Kanrar S, Lee B, Hong X, Agarwal M, Zhu JK (2014) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054
Chou WL, Huang LF, Fang JC, Yeh CH, Hong CY, Wu SJ, Lu CA (2014) Divergence of the expression and subcellular localization of CCR4-associated factor 1 (CAF1) deadenylase proteins in Oryza sativa. Plant Mol Biol 85:443–458
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676
Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326
Crosatti C, de Laureto PP, Bassi R, Cattivelli L (1999) The interaction between cold and light controls the expression of the cold-regulated barley gene cor14b and the accumulation of the corresponding protein. Plant Physiol 119:671–680
De Biaggi M (2005) Rhizomania. In: Biancardi E, Campbell LG, Skaracis GN, De Biaggi M (eds) genetics and breeding of sugar beet. Science Publisher, Enfield, pp 80–85
Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol 10:151. doi:10.1186/1471-2229-10-151
Dohm JC, Minoche AE, Holtgräwe D, Capella-Gutiérrez S, Zakrzewski F, Tafer H, Rupp O, Rosleff Sörensen T, Stracke R, Reinhardt R, Goesmann A, Kraft T, Schulz B, Stadler PF, Schmidt T, Gabaldón T, Lehrach H, Weisshaar B, Himmelbauer H (2013) The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505:546–549
Fowler SG, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690
Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137:961–968
Franklin KA, Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 39:1410–1414
Fuchs S, Grill E, Meskiene I, Schweighofer A (2013) Type 2C protein phosphatases in plants. FEBS J 280:681–693
Ganeshan S, Vitamvas P, Fowler DB, Chibbar RN (2008) Quantitative expression analysis of selected COR genes reveals their differential expression in leaf and crown tissues of wheat (Triticum aestivum L.) during an extended low temperature acclimation regimen. J Exp Bot 59:2393–2402
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652
Griffith M, Lumb C, Wiseman SB, Wisniewski M, Johnson RW, Marangoni AJ (2005) Antifreeze proteins modify the freezing process in planta. Plant Physiol 138:1330–1340
Gusta LV, Wisniewski M (2013) Understanding cold hardiness: an opinion. Physiol Plant 147:4–14
Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 1:179–196
Harrison MA (2012) Cross-talk between phytohormone signaling pathways under both optimal and stressful environmental conditions. In: Khan NA et al (eds) Phytohormones and abiotic stress tolerance in plants. Springer, Berlin, pp 49–76
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Stn 347:1–32
Hoffman CM (2010) Root quality of sugar beet. Sugar Tech 12:276–287
Huang X, Li J, Bao F, Zhang X, Yang S (2010) A gain-of-function mutation in the Arabidopsis disease resistance gene RPP4 confers sensitivity to low temperature. Plant Physiol 154:796–809
Jensen JK, Johnson N, Wilkerson CG (2013) Discovery of diversity in xylan biosynthetic genes by transcriptional profiling of a heteroxylan containing mucilaginous tissue. Front Plant Sci 4:183. doi:10.3389/fpls.2013.00183
Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS (1996) Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci USA 93:11274–11279
Kirchhoff M, Svirshchevskaya A, Hoffman C, Schechert A, Jung C, Kopisch-Obuch F (2012) High degree of genetic variation of winter hardiness in a panel of Beta vulgaris L. Crop Sci 52:179–188
Knight MR, Knight H (2012) Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 195:737–751
Lee B, Henderson DA, Zhu J (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175
Levitt J (1980) Response of plants to environmental stresses. 2nd edn. I. Chilling, freezing and high temperature stresses. Academic Press, New York
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323
Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649
Loel J, Hoffmann CM (2014) Importance of growth stage and weather conditions for the winter hardiness of autumn sown sugar beet. Field Crops Res 162:70–76
Mao Y, Pavangadkar KA, Thomashow MF, Triezenberg SJ (2006) Physical and functional interactions of Arabidopsis ADA2 transcriptional coactivator proteins with the acetyltransferase GCN5 and with the cold-induced transcription factor CBF1. Biochim Biophys Acta 1759:69–79
Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a Tiling array. Plant Cell Physiol 49:1135–1149
Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96
Mutasa-Göttgens ES, Joshi A, Holmes HF, Hedden P, Göttgens B (2012) A new RNASeq-based reference transcriptome for sugar beet and its application in transcriptome-scale analysis of vernalization and gibberellin responses. BMC Genom 13:99
Pacifico D, Onofri C, Mandolino G (2011) Cold-modulated expression of genes encoding for key enzymes of the sugar metabolism in spring and autumn cvs. of Beta vulgaris L. Plant Genet Resour 9:268–271
Panella LW, Lewellen RT (2007) Broadening the genetic base of sugar beet: introgression from wild relatives. Euphytica 154:383–400
Park S, Lee C-M, Doherty CJ, Gilmour SJ, Kim YS, Thomashow MF (2015) Regulation of Arabidopsis CBF regulon by a complex low temperature regulatory network. Plant J. doi:10.1111/tpj.12796
Pestsova P, Meinhard J, Menze A, Fischer U, Windhövel A, Westhoff P (2008) Transcript profiles uncover temporal and stress-induced changes of metabolic pathways in germinating sugar beet seeds. BMC Plant Biol 8:122
Pulido P, Perello C, Rodriguez-Conception M (2012) New insights into plant isoprenoid metabolism. Mol Plant 5:964–967
Qi B, Yang Y, Yin Y, Xu M, Li H (2014) De novo sequencing, assembly, and analysis of the Taxodium ‘Zhongshansa’ roots and shoots transcriptome in response to short-term waterlogging. BMC Plant Biol 14:201
Reeves PA, He Y, Schmitz RJ, Amasino RM, Panella LW, Richards CM (2007) Evolutionary conservation of the FLOWERING LOCUS C-mediated vernalization response: evidence from the sugar beet (Beta vulgaris). Genetics 176:295–307
Reinsdorf E, Koch HJ, Märlander B (2013) Phenotype related differences in frost tolerance of winter sugar beet (Beta vulgaris L.). Field Crops Res 151:27–34
Rohloff J, Kopka J, Erban A, Winge P, Wilson RC, Bones AM, Davik J, Randall SK, Alsheik MK (2012) Metabolite profiling reveals novel multi-level cold responses in the diploid model Fragaria vesca (woodland strawberry). Phytochemistry 77:99–109
Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokreis M, Tetko I, Güldener U, Mannhaupt G, Münsterkötter M, Mewes HW (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32:5539–5545
Sasidharan R, Voesenek LA, Pierik R (2011) Cell wall modifying proteins mediate plant acclimatization to biotic and abiotic stresses. CRC Crit Rev Plant Sci 30:548–562
Skaracis GN, Biancardi E (2005) Cercospora leaf spot. In: Biancardi E, Campbell LG, Skaracis GN, De Biaggi M (eds) Genetics and breeding of sugar beet. Science Publisher, Enfield, pp 88–90
Snider CS, Hsiang T, Zhao G, Griffith M (2000) Role of ice nucleation and antifreeze activities in pathogenesis and growth of snow molds. Phytopathology 90:354–361
Soitamo AJ, Piippo M, Allahverdiyeva Y, Battchikova N, Aro EM (2008) Light has a specific role in modulating Arabidopsis gene expression at low temperature. BMC Plant Biol 8:13
Stevanato P (2005) Resistance to abiotic stresses. In: Biancardi E, Campbell LG, Skaracis GN, De Biaggi M (eds) Genetics and breeding of sugar beet. Science Publisher Inc., USA, pp 116–119
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:570–599
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515
Turesson H, Andersson M, Marttila S, Thulin I, Hofvander P (2014) Starch biosynthetic genes and enzymes are expressed and active in the absence of starch accumulation in sugar beet tap-root. BMC Plant Biol 14:104
Vastarelli P, Moschella A, Pacifico D, Mandolino G (2013) Water stress in Beta vulgaris: osmotic adjustment response and gene expression analysis in ssp. vulgaris and maritima. Am J Plant Sci 4:11–16
Vlachonasios KE, Thomashow MF, Triezenberg SJ (2003) Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development and gene expression. Plant Cell 15:626–638
Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol 8:749–771
Wood RR (1952) Selection for cold tolerance and low temperature germination in sugar beets. In: Proceedings of the General Meeting of the Am. Soc. Sugar Beet Technologists, pp 407–410
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low temperature, or high-salt stress. Plant Cell 6:251–264
Yang CJ, Zhang C, Lu YN, Jin JQ, Wang XL (2011) The mechanisms of brassinosteroids’ action: from signal transduction to plant development. Mol Plant 4:588–600
Yoon GM, Kleber JJ (2013) 1-aminocyclopropane-1-carboxylic acid as a signalling molecule in plants. AoB Plants 5:plt017. doi:10.1093/aobpla/plt017
Zhu J, Lee B, Dellinger M, Cui X, Zhang C, Wu S, Nothnagel EA, Zhu J (2010a) A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis. Plant J 63:128–140
Zhu Y, Qian W, Hua J (2010b) Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog 6:e1000844. doi:10.1371/journal.ppat.1000844
Acknowledgments
The present work was funded by the Italian Ministry of Agriculture and Forestry (MIPAF), in the frame of the research project “Agronanotech, Le nuove tecnologie molecolari per l’analisi del genoma di organismi di interesse agrario”. The authors wish to thank dr. Enrico Biancardi (CRA-Research Center for Industrial Crops, Rovigo) for providing helpful discussion on sugar beet stress physiology and genetics and for seeds of the sugar beet cv. Bianca.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
425_2015_2299_MOESM1_ESM.pdf
Electronic Supplementary Material S1 (ESM 1) Distribution of FPKM values as a function of the number of contigs in control leaves and roots (PDF 74 kb)
425_2015_2299_MOESM3_ESM.pdf
Electronic Supplementary Material S3 (ESM 3) Summary of all significantly DE transcription factors in leaves and roots (PDF 59 kb)
Rights and permissions
About this article
Cite this article
Moliterni, V.M.C., Paris, R., Onofri, C. et al. Early transcriptional changes in Beta vulgaris in response to low temperature. Planta 242, 187–201 (2015). https://doi.org/10.1007/s00425-015-2299-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-015-2299-z