Abstract
Previous studies have indicated that hormonal control is essential for plant root growth. The root of the carrot is an edible vegetable with a high nutritional value. However, molecular mechanisms underlying hormone-mediated root growth of carrot have not been illustrated. Therefore, the present study collected carrot root samples from four developmental stages, and performed transcriptome sequencing to understand the molecular functions of plant hormones in carrot root growth. A total of 160,227 transcripts were generated from our transcriptome, which were assembled into 32,716 unigenes with an average length of 1,453 bp. A total of 4,818 unigenes were found to be differentially expressed between the four developmental stages. In total, 87 hormone-related differentially expressed genes were identified, and the roles of the hormones are extensively discussed. Our results suggest that plant hormones may regulate carrot root growth in a phase-dependent manner, and these findings will provide valuable resources for future research on carrot root development.
Similar content being viewed by others
References
Aloni R (2013) Role of hormones in controlling vascular differentiation and the mechanism of lateral root initiation. Planta 238:819–830
Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann Bot 97:883–893
Ando K, Carr K, Grumet R (2012) Transcriptome analyses of early cucumber fruit growth identifies distinct gene modules associated with phases of development. BMC Genomics 13:518
Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44
Creelman RA (1998) Jasmonate perception: characterization of COI1 mutants provides the first clues. Trends Plant Sci 3:367–368
Duarte J, Rivière N, Baranger A, Aubert G, Burstin J, Cornet L, Lavaud C, Lejeune-Hénaut I, Martinant JP, Pichon JP, Pilet-Nayel ML, Boutet G (2014) Transcriptome sequencing for high throughput SNP development and genetic mapping in Pea. BMC Genomics 15:126
Durbak A, Yao H, McSteen P (2012) Hormone signaling in plant development. Curr Opin Plant Biol 15:92–96
Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12:1117–1126
Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S (2011) Brassinosteroid perception in the epidermis controls root meristem size. Development 138:839–848
Herder GD, Van Isterdael G, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends Plant Sci 15:600–607
Huang Y, Li MY, Wang F, Xu ZS, Huang W, Wang GL, Ma J, Xiong AS (2014) Heat shock factors in carrot: genome-wide identification, classification, and expression profiles response to abiotic stress. Mol Biol Rep. doi:10.1007/s11033-11014-13826-x
Inada S, Shimmen T (2000) Regulation of elongation growth by gibberellin in root segments of Lemna minor. Plant Cell Physiol 41:932–939
Joshi-Saha A, Valon C, Leung J (2011) Abscisic acid signal off the STARTing block. Mol Plant 4:562–580
Jung JKH, McCouch S (2013) Getting to the roots of it: genetic and hormonal control of root architecture. Front Plant Sci 4:186
Klaus M, Aaron L, Thomas E, Allen M, Jürg S, Kay AL, Jeffery LD, Robert AD (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26:403–410
Kuderová A, Urbánková I, Válková M, Malbeck J, Brzobohatý B, Némethová D, Hejátko J (2008) Effects of conditional IPT-dependent cytokinin overproduction on root architecture of Arabidopsis seedlings. Plant Cell Physiol 49:570–582
Kulka RG (2008) Hormonal control of root development on epiphyllous plantlets of Bryophyllum (Kalanchoë) marnierianum: role of auxin and ethylene. J Exp Bot 59:2361–2370
LeClere S, Schmelz EA, Chourey PS (2010) Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiol 153:306–318
Li MY, Wang F, Jiang Q, Ma J, Xiong AS (2014) Identification of SSRs and differentially expressed genes in two cultivars of celery (Apium graveolens L.) by deep transcriptome sequencing. Hort Res 1:10
Liu J, Rowe J, Lindsey K (2014) Hormonal crosstalk for root development: a combined experimental and modeling perspective. Front Plant Sci 5:116
López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Pérez-Torres A, Rampey RA, Bartel B, Herrera-Estrella L (2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol 137:681–691
Lou Q, Liu Y, Qi Y, Jiao S, Tian F, Jiang L, Wang Y (2014) Transcriptome sequencing and metabolite analysis reveals the role of delphinidin metabolism in flower colour in grape hyacinth. J Exp Bot 65:3157–3164
Lu T, Lu G, Fan D, Zhu C, Li W, Zhao Q, Feng Q, Zhao Y, Guo Y, Li W, Huang X, Han B (2010) Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res 20:1238–1249
Luby CH, Maeda HA, Goldman IL (2014) Genetic and phenological variation of tocochromanol (vitamin E) content in wild (Daucus carota L. var. carota) and domesticated carrot (D. carota L. var. sativa). Hort Res 1:15
Luo X, Chen Z, Gao J, Gong Z (2014) Abscisic acid inhibits root growth in Arabidopsis through ethylene biosynthesis. Plant J 79:44–55
Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77
Michalczuk L, Cooke TJ, Cohen JD (1992) Auxin levels at different stages of carrot somatic embryogenesis. Phytochemistry 31:1097–1103
Mitsuhashi W, Toyomasu T, Masui H, Katho T, Nakaminami K, Kashiwagi Y, Akutsu M, Kenmoku H, Sassa T, Yamaguchi S, Kamiya Y, Kamada H (2003) Gibberellin is essentially required for carrot (Daucus carota L.) somatic embryogenesis: dynamic regulation of gibberellin 3-oxidase gene expressions. Biosci Biotechnol Biochem 67:2438–2447
Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443:458–461
Müssig C, Shin G-H, Altmann T (2003) Brassinosteroids promote root growth in Arabidopsis. Plant Physiol 133:1261–1271
Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475
Perilli S, Di Mambro R, Sabatini S (2012) Growth and development of the root apical meristem. Curr Opin Plant Biol 15:17–23
Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590
Reed RC, Brady SR, Muday GK (1998) Inhibition of auxin movement from the shoot into the root Inhibits lateral root development in Arabidopsis. Plant Physiol 118:1369–1378
Remans T, Thijs S, Truyens S, Weyens N, Schellingen K, Keunen E, Gielen H, Cuypers A, Vangronsveld J (2012) Understanding the development of roots exposed to contaminants and the potential of plant-associated bacteria for optimization of growth. Ann Bot 110:239–252
Ren B, Liang Y, Deng Y, Chen Q, Zhang J, Yang X, Zuo J (2009) Genome-wide comparative analysis of type-A Arabidopsis response regulator genes by overexpression studies reveals their diverse roles and regulatory mechanisms in cytokinin signaling. Cell Res 19:1178–1190
Rich SM, Watt M (2013) Soil conditions and cereal root system architecture: review and considerations for linking Darwin and Weaver. J Exp Bot 64:1193–1208
Saini S, Sharma I, Kaur N, Pati P (2013) Auxin: a master regulator in plant root development. Plant Cell Rep 32:741–757
Schiefelbein JW, Benfey PN (1991) The development of plant roots: new approaches to underground problems. Plant Cell 3:1147–1154
Shan X, Zhang Y, Peng W, Wang Z, Xie D (2009) Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J Exp Bot 60:3849–3860
Shani E, Weinstain R, Zhang Y, Castillejo C, Kaiserli E, Chory J, Tsien RY, Estelle M (2013) Gibberellins accumulate in the elongating endodermal cells of Arabidopsis root. Proc Natl Acad Sci USA 110:4834–4839
Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55:2343–2351
Singh VK, Garg R, Jain M (2013) A global view of transcriptome dynamics during flower development in chickpea by deep sequencing. Plant Biotechnol J 11:691–701
Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43
Sweetman C, Wong D, Ford C, Drew D (2012) Transcriptome analysis at four developmental stages of grape berry (Vitis vinifera cv. Shiraz) provides insights into regulated and coordinated gene expression. BMC Genom 13:691
Takatsuka H, Umeda M (2014) Hormonal control of cell division and elongation along differentiation trajectories in roots. J Exp Bot 65:2633–2643
Titapiwatanakun B, Murphy AS (2009) Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. J Exp Bot 60:1093–1107
Torti S, Fornara F, Vincent C, Andrés F, Nordström K, Göbel U, Knoll D, Schoof H, Coupland G (2012) Analysis of the Arabidopsis shoot meristem transcriptome during floral transition identifies distinct regulatory patterns and a leucine-rich repeat protein that promotes flowering. Plant Cell 24:444–462
Ubeda-Tomás S, Federici F, Casimiro I, Beemster GTS, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ (2009) Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 19:1194–1199
Vilaine F, Kerchev P, Clément G, Batailler B, Cayla T, Bill L, Gissot L, Dinant S (2013) Increased expression of a phloem membrane protein encoded by NHL26 alters phloem export and sugar partitioning in Arabidopsis. Plant Cell 25:1689–1708
Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550
Woeste KE, Ye C, Kieber JJ (1999) Two Arabidopsis mutants that overproduce ethylene are affected in the posttranscriptional regulation of 1-aminocyclopropane-1-carboxylic acid synthase. Plant Physiol 119:521–530
Wu W, Cheng S (2014) Root genetic research, an opportunity and challenge to rice improvement. Field Crop Res 165:111–124
Xu ZS, Huang Y, Wang F, Song X, Wang GL, Xiong AS (2014a) Transcript profiling of structural genes involved in cyanidin-based anthocyanin biosynthesis between purple and non-purple carrot (Daucus carota L.) cultivars reveals distinct patterns. BMC Plant Biol 14:262
Xu ZS, Tan HW, Wang F, Hou XL, Xiong AS (2014) CarrotDB: a genomic and transcriptomic database for carrot. Database 2014:bau096
Yokoyama A, Yamashino T, Amano Y-I, Tajima Y, Imamura A, Sakakibara H, Mizuno T (2007) Type-B ARR transcription factors, ARR10 and ARR12, are implicated in cytokinin-mediated regulation of protoxylem differentiation in roots of Arabidopsis thaliana. Plant Cell Physiol 48:84–96
Zhou ZY, Zhang CG, Wu L, Zhang CG, Chai J, Wang M, Jha A, Jia PF, Cui SJ, Yang M, Chen R, Guo GQ (2011) Functional characterization of the CKRC1/TAA1 gene and dissection of hormonal actions in the Arabidopsis root. Plant J 66:516–527
Acknowledgments
The research was supported by the New Century Excellent Talents in University (NCET-11-0670); Jiangsu Natural Science Foundation (BK20130027); China Postdoctoral Science Foundation (2014M551609), Priority Academic Program Development of Jiangsu Higher Education Institutions Project.
Conflict of interest
The authors declare that there are no competing interests.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S.Hohmann.
Rights and permissions
About this article
Cite this article
Wang, GL., Jia, XL., Xu, ZS. et al. Sequencing, assembly, annotation, and gene expression: novel insights into the hormonal control of carrot root development revealed by a high-throughput transcriptome. Mol Genet Genomics 290, 1379–1391 (2015). https://doi.org/10.1007/s00438-015-0999-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-015-0999-5