Abstract
Development of storage roots is a process associated with a phase change from cell division and elongation to radial growth and accumulation of massive amounts of reserve substances such as starch. Knowledge of the regulation of cassava storage root formation has accumulated over time; however, gene regulation during the initiation and early stage of storage root development is still poorly understood. In this study, transcription profiling of fibrous, intermediate and storage roots at eight weeks old were investigated using a 60-mer-oligo microarray. Transcription and gene expression were found to be the key regulating processes during the transition stage from fibrous to intermediate roots, while homeostasis and signal transduction influenced regulation from intermediate roots to storage roots. Clustering analysis of significant genes and transcription factors (TF) indicated that a number of phytohormone-related TF were differentially expressed; therefore, phytohormone-related genes were assembled into a network of correlative nodes. We propose a model showing the relationship between KNOX1 and phytohormones during storage root initiation. Exogeneous treatment of phytohormones N 6-benzylaminopurine and 1-Naphthaleneacetic acid were used to induce the storage root initiation stage and to investigate expression patterns of the genes involved in storage root initiation. The results support the hypothesis that phytohormones are acting in concert to regulate the onset of cassava storage root development. Moreover, MeAGL20 is a factor that might play an important role at the onset of storage root initiation when the root tip becomes swollen.
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References
Achard P, Baghour M, Chapple A, Hedden P, Van Der Straeten D (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc Natl Acad Sci USA 104:6484–6489
An D, Yang J, Zhang P (2012) Transcriptome profiling of low temperature-treated cassava apical shoots showed dynamic responses of tropical plant to cold stress. BMC Genom 13:64
Baud S, Vaultier MN, Rochat C (2004) Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 55:397–409. doi:10.1093/jxb/erh047
Chang W-C, Lee T-Y, Huang H-D, Huang H-Y, Pan R-L (2008) PlantPAN: plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genom 9:561
Chen H, Rosin FM, Prat S, Hannapel DJ (2003) Interacting transcription factors from the three-amino acid loop extension superclass regulate tuber formation. Plant Physiol 132:1391–1404. doi:10.1104/pp.103.022434
Chen H, Banerjee AK, Hannapel DJ (2004) The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J 38:276–284. doi:10.1111/j.1365-313X.2004.02048.x
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. doi:10.1093/bioinformatics/bti610
Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17:678–682. doi:10.1016/j.cub.2007.02.047
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70. doi:10.1093/nar/gkq310
Eguchi T, Yoshida S (2008) Effects of application of sucrose and cytokinin to roots on the formation of tuberous roots in sweetpotato (Ipomoea batatas (L.) Lam.). Plant Root 2:7–13
Enami K, Ozawa T, Motohashi N, Nakamura M, Tanaka K, Hanaoka M (2011) Plastid-to-nucleus retrograde signals are essential for the expression of nuclear starch biosynthesis genes during amyloplast differentiation in tobacco BY-2 cultured cells. Plant Physiol 157:518–530. doi:10.1104/pp.111.178897
Firon N et al (2013) Transcriptional profiling of sweetpotato (Ipomoea batatas) roots indicates down-regulation of lignin biosynthesis and up-regulation of starch biosynthesis at an early stage of storage root formation. BMC Genom 14:460
Fleet CM, Sun T-p (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85. doi:10.1016/j.pbi.2004.11.015
González-Schain ND, Díaz-Mendoza M, Żurczak M, Suárez-López P (2012) Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner. Plant J 70:678–690. doi:10.1111/j.1365-313X.2012.04909.x
Goodstein DM et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186. doi:10.1093/nar/gkr944
Guo D, Chen F, Inoue K, Blount JW, Dixon RA (2001) Downregulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa: impacts on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell Online 13:73–88. doi:10.1105/tpc.13.1.73
Hajirezaei M-R, Biemelt S, Peisker M, Lytovchenko A, Fernie AR, Sonnewald U (2006) The influence of cytosolic phosphorylating glyceraldehyde 3-phosphate dehydrogenase (GAPC) on potato tuber metabolism. J Exp Bot 57:2363–2377. doi:10.1093/jxb/erj207
Hannapel DJ (2007) Signaling the induction of tuber formation . In: Gebhardt C, Bradshaw J, Govers F, MacKerron DKL, Taylor MA, Ross HA (eds) Potato biology and biotechnology: advanes and perspectives. Elsevier, New York, pp 237–256
Hwang I, Sheen J, Müller B (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63:353–380. doi:10.1146/annurev-arplant-042811-105503
Ioio RD, Linhares FS, Sabatini S (2008) Emerging role of cytokinin as a regulator of cellular differentiation. Curr Opin Plant Biol 11:23–27. doi:10.1016/j.pbi.2007.10.006
Ku AT, Huang Y-S, Wang Y-S, Ma D, Yeh K-W (2008) IbMADS1 (Ipomoea batatas MADS-box 1 gene) is involved in tuberous root initiation in sweet potato (Ipomoea batatas). Ann Bot 102:57–67. doi:10.1093/aob/mcn067
Li X-Q, Zhang D (2003) Gene expression activity and pathway selection for sucrose metabolism in developing storage root of sweet potato. Plant Cell Physiol 44:630–636. doi:10.1093/pcp/pcg080
Li Y-Z et al (2010) An ordered EST catalogue and gene expression profiles of cassava (Manihot esculenta) at key growth stages. Plant Mol Biol 74:573–590. doi:10.1007/s11103-010-9698-0
Liu X et al (2008) Genome-wide analysis of gene expression profiles during the kernel development of maize (Zea mays L.). Genomics 91:378–387. doi:10.1016/j.ygeno.2007.12.002
McGregor CE (2006) Differential expression and detection of transcripts in sweetpotato (Ipomoea batatas (L.) LAM.) using cDNA microarrays. Louisiana State University, Louisiana
Medina RD, Faloci MM, Gonzalez AM, Mroginski LA (2007) In vitro cultured primary roots derived from stem segments of cassava (Manihot esculenta) can behave like storage organs. Ann Bot 99:409–423. doi:10.1093/aob/mcl272
Miyazawa Y, Sakai A, S-y Miyagishima, Takano H, Kawano S, Kuroiwa T (1999) Auxin and cytokinin have opposite effects on amyloplast development and the expression of starch synthesis genes in cultured bright yellow-2 tobacco cells. Plant Physiol 121:461–470. doi:10.1104/pp.121.2.461
Muñoz-Bertomeu J et al (2009) Plastidial glyceraldehyde-3-phosphate dehydrogenase deficiency leads to altered root development and affects the sugar and amino acid balance in arabidopsis. Plant Physiol 151:541–558. doi:10.1104/pp.109.143701
Nakajima K, Furutani I, Tachimoto H, Matsubara H, Hashimoto T (2004) SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding arabidopsis cells. Plant Cell Online 16:1178–1190. doi:10.1105/tpc.017830
Noh SA, Lee H-S, Huh EJ, Huh GH, Paek K-H, Shin JS, Bae JM (2010) SRD1 is involved in the auxin-mediated initial thickening growth of storage root by enhancing proliferation of metaxylem and cambium cells in sweetpotato (Ipomoea batatas). J Exp Bot 61:1337–1349. doi:10.1093/jxb/erp399
Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol. doi:10.1101/cshperspect.a001537
Pawitan Y, Michiels S, Koscielny S, Gusnanto A, Ploner A (2005) False discovery rate, sensitivity and sample size for microarray studies. Bioinformatics 21:3017–3024. doi:10.1093/bioinformatics/bti448
Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harbor Perspectives in Biology. doi:10.1101/cshperspect.a001446
Prammanee S, Kamprerasart K, Salakan S, Sriroth K (2010) Growth and starch content evaluation on newly released cassava cultivars, Rayong 9, Rayong 7 and Rayong 80 at different harvest times. Kasetsart J (Nat Sci) 44:558–563
Q-m Wang, L-m Zhang, Y-a Guan, Z-l Wang (2006) Endogenous hormone concentration in developing tuberous roots of different sweet potato genotypes. Agric Sci China 5:919–927. doi:10.1016/S1671-2927(07)60005-4
Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc Natl Acad Sci 103:11081–11085. doi:10.1073/pnas.0602038103
Ravi V, Chakrabarti SK, Makeshkumar T, Saravanan R (2014) Molecular Regulation of Storage Root Formation and Development in Sweet Potato. In: Horticultural reviews, volume 42. Wiley, pp 157–208. doi:10.1002/9781118916827.ch03
Reilly K, Bernal D, Cortés D, Gómez-Vásquez R, Tohme J, Beeching J (2007) Towards identifying the full set of genes expressed during cassava post-harvest physiological deterioration. Plant Mol Biol 64:187–203. doi:10.1007/s11103-007-9144-0
Rodriguez-Falcon M, Bou J, Prat S (2006) Seasonal control of tuberization in potato: conserved elements with the flowering response. Annu Rev Plant Biol 57:151–180. doi:10.1146/annurev.arplant.57.032905.105224
Rosin FM, Hart JK, Horner HT, Davies PJ, Hannapel DJ (2003) Overexpression of a knotted-like homeobox gene of potato alters vegetative development by decreasing gibberellin accumulation. Plant Physiol 132:106–117. doi:10.1104/pp.102.015560
Roumeliotis E, Kloosterman B, Oortwijn M, Kohlen W, Bouwmeester HJ, Visser RGF, Bachem CWB (2012a) The effects of auxin and strigolactones on tuber initiation and stolon architecture in potato. J Exp Bot 63:4539–4547. doi:10.1093/jxb/ers132
Roumeliotis E, Visser RGF, Bachem CWB (2012b) A crosstalk of auxin and GA during tuber development. Landes Biosci 7:1360–1363
Rouse-Miller J, Bowrin V, Sirju-Charran G, Sutton F (2013) Inverse oriented stem cuttings generate tuberous stems in cassava Manihot esculenta Crantz; an alternative sink site. J Plant Biochem Physiol 1:117. doi:10.4172/2329-9029.1000117
Sakamoto T, Kobayashi M, Itoh H, Tagiri A, Kayano T (2001) Expression of a gibberellin 2-oxidase gene around the shoot apex is related to phase transition in rice. Plant Physiol 125:1508–1516
Sakurai T et al (2007) Sequencing analysis of 20,000 full-length cDNA clones from cassava reveals lineage specific expansions in gene families related to stress response. BMC Plant Biol 7:66
Scanlon MJ, Henderson DC, Bernstein B (2002) SEMAPHORE1 functions during the regulation of ancestrally duplicated knox genes and polar auxin transport in maize. Development 129:2663–2673
Sergeeva LI, De Bruijn SM, Koot-Gronsveld EAM, Navratil O, Vreugdenhil D (2000) Tuber morphology and starch accumulation are independent phenomena: evidence from ipt-transgenic potato lines. Physiol Plant 108:435–443. doi:10.1034/j.1399-3054.2000.100414.x
Sheffield J, Taylor N, Fauquet C, Chen S (2006) The cassava (Manihot esculenta Crantz) root proteome: protein identification and differential expression. Proteomics 6:1588–1598
Siriwat W, Kalapanulak S, Suksangpanomrung M, Netrphan S, Meechai A, Saithong T (2012) Transcriptomic data integration inferring the dominance of starch biosynthesis in carbon utilization of developing cassava roots. Proc Comput Sci 11:96–106. doi:10.1016/j.procs.2012.09.011
Smith OE, Palmer CE (1970) Cytokinin-cytokinin-induced tuber formation tuber formation on stolons of Solanum tuberosum. Physiol Plant 23:599–606. doi:10.1111/j.1399-3054.1970.tb06452.x
Sturm A, Tang G-Q (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407. doi:10.1016/S1360-1385(99)01470-3
Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18:207–208. doi:10.1093/bioinformatics/18.1.207
Tanaka M, Kato N, Nakayama H, Nakatani M, Takahata Y (2008) Expression of class I knotted1-like homeobox genes in the storage roots of sweetpotato (Ipomoea batatas). J Plant Physiol 165:1726–1735
Teerawanichpan P, Lertpanyasampatha M, Netrphan S, Varavinit S, Boonseng O, Narangajavana J (2008) Influence of cassava storage root development and environmental conditions on starch granule size distribution. Starch Stärke 60:696–705. doi:10.1002/star.200800226
Testone G et al (2012) The peach (Prunus persica L. Batsch) genome harbours 10 KNOX genes, which are differentially expressed in stem development, and the class 1 KNOPE1 regulates elongation and lignification during primary growth. J Exp Bot 63:5417–5435. doi:10.1093/jxb/ers194
Townsley BT, Sinha NR, Kang J (2013) KNOX1 genes regulate lignin deposition and composition in monocots and dicots. Front Plant Sci. doi:10.3389/fpls.2013.00121
Tsai Y-C et al (2012) Characterization of genes involved in cytokinin signaling and metabolism from rice. Plant Physiol 158:1666–1684. doi:10.1104/pp.111.192765
Tsiantis M, Brown MIN, Skibinski G, Langdale JA (1999) Disruption of auxin transport is associated with aberrant leaf development in maize. Plant Physiol 121:1163–1168. doi:10.1104/pp.121.4.1163
Utsumi Y et al (2012) Transcriptome analysis using a high-density oligomicroarray under drought stress in various genotypes of cassava: an important tropical crop. DNA Res 19:335–345. doi:10.1093/dnares/dss016
Watillon B, Kettmann R, Boxus P, Burny A (1991) Characterization of two gene transcripts modulated by cytokinins in micropropagated apple (Malus domestica [L.] Borkh) plantlets. Plant Physiol 96:479–484
Willige BC, Isono E, Richter R, Zourelidou M, Schwechheimer C (2011) Gibberellin regulates PIN-FORMED abundance and is required for auxin transport-dependent growth and development in arabidopsis thaliana. Plant Cell Online 23:2184–2195. doi:10.1105/tpc.111.086355
Xu X, van Lammeren AAM, Vermeer E, Vreugdenhil D (1998) The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro. Plant Physiol 117:575–584. doi:10.1104/pp.117.2.575
Yang J, An D, Zhang P (2011) Expression profiling of cassava storage roots reveals an active process of glycolysis/gluconeogenesis. J Integr Plant Biol 53:193–211
You MK, Hur CG, Ahn YS, Suh MC, Jeong BC, Shin JS, Bae JM (2003) Identification of genes possibly related to storage root induction in sweetpotato. FEBS Lett 536:101–105. doi:10.1016/s0014-5793(03)00035-8
Zhang W, To JPC, Cheng C-Y, Eric Schaller G, Kieber JJ (2011) Type-A response regulators are required for proper root apical meristem function through post-transcriptional regulation of PIN auxin efflux carriers. Plant J 68:1–10. doi:10.1111/j.1365-313X.2011.04668.x
Acknowledgments
This work was partially supported by (1) Faculty of Science, Mahidol University, Thailand (2) The Thailand Research Fund (RSA5780030), Thailand and (3) RIKEN Center for Sustainable Resource Science under the Strategic Funds for the Promotion of Science and Technology of the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan. We thank Dr. Opas Boonseng (Rayong Field Crops Research Center, Ministry of Agriculture and Cooperatives, Rayong, Thailand) for KU50 field experiments, Assist. Prof. Paweena Traiperm (Department of Plant Science, Faculty of Science, Mahidol University, Bangkok, Thailand) for assistance in microscopic works, and Ms Somkid Bumee (Systems Biology and Bioinformatics Laboratory, Pilot Plant Development and Training Institute, King Mongkut’s University of Technology, Bangkok, Thailand) for computational support.
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Sojikul, P., Saithong, T., Kalapanulak, S. et al. Genome-wide analysis reveals phytohormone action during cassava storage root initiation. Plant Mol Biol 88, 531–543 (2015). https://doi.org/10.1007/s11103-015-0340-z
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DOI: https://doi.org/10.1007/s11103-015-0340-z