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Dynamic changes in carbohydrate metabolism and endogenous hormones during Tulipa edulis stolon development into a new bulb

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Abstract

The stolon is the main asexual reproductive organ of Tulipa edulis (Miq.) Baker. It has a special morphology and can develop into a new bulb for propagation. In the current greenhouse experiment, the dynamic changes in carbohydrates and related enzymes, protein and endogenous hormones during T. edulis stolon development were investigated. The results showed that soluble sugar levels were basically declining, whereas starch and protein content rose continuously during stolon development. The adenosine diphosphoglucose pyrophosphorylase (AGPase) activity peaked in the initial swelling stage and stayed a relative high level in the middle swelling stage; sucrose synthase (SS), soluble starch synthase (SSS) and granule-bound starch synthase (GBSS) activities followed the same law that showed rising trends during stolon development. SS activity was significantly inversely related to sucrose content but had significantly positive relations with starch content, SSS and GBSS activities. Gibberellin (GA), indole-3-acetic acid (IAA) and zeatin riboside (ZR) peaked in the initial swelling stage and maintained high levels in the middle swelling stage; they then decreased significantly in the later swelling stage. A substantial increase was observed in abscisic acid (ABA) content until the middle swelling stage, followed by a significant reduction in the later swelling stage. The ratios of ABA to IAA, GA and ZR reached their lowest levels in the initial swelling stage. In conclusion, T. edulis stolon development is a process of new bulb morphogenesis along with the starch accumulation catalyzed by AGPase, SSS and GBSS, using the product of sucrose cleavage caused by SS. Initial low ABA content and low ratios of ABA to IAA, GA and ZR, together with the GA, IAA and ZR of high-content, soluble sugars worked more efficiently to induce new bulb formation.

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References

  • Abdul Jaleel C, Kishorekumar A, Manivannan P, Sankar B, Gomathinayagam M, Gopi R, Somasundaram R, Panneerselvam R (2007) Alterations in carbohydrate metabolism and enhancement in tuber production in white yam (Dioscorea rotundata Poir.) under triadimefon and hexaconazole applications. Plant Growth Regul 53:7–16

    Article  Google Scholar 

  • Aksenova NP, Sergeeva LI, Kolachevskaya OO, Romanov GA (2014) Hormonal regulation of tuber formation in potato, In KG Ramawat, JM Merillon, eds, Bulbous Plants, Biotechnology. CRC Press, New York, Oxon UK, pp 3–36

    Google Scholar 

  • Bakhshaie M, Babalar M, Mirmasoumi M, Khalighi A (2010) Somatic embryogenesis and plant regeneration of Lilium ledebourii (Baker) Boiss., an endangered species. Plant Cell Tiss Org 102:229–235

    Article  CAS  Google Scholar 

  • Baroja-Fernández E, Muñoz FJ, Montero M, Etxeberria E, Sesma MT, Ovecka M, Bahaji A, Ezquer I, Li J, Prat S, Pozueta Romero J (2009) Enhancing sucrose synthase activity in transgenic potato (Solanum tuberosum L.) tubers results in increased levels of starch, ADPglucose and UDPglucose and total yield. Plant Cell Physiol 50:1651–1662

    Article  PubMed  Google Scholar 

  • Baroja-Fernández E, Muñoz FJ, Saikusa T, Rodríguez-López M, Akazawa T, Pozueta-Romero J (2003) Sucrose synthase catalyzes the de novo production of ADPglucose linked to starch biosynthesis in heterotrophic tissues of plants. Plant Cell Physiol 44:500–509

    Article  PubMed  Google Scholar 

  • Bing QZ, Zhang BG, Zhang Z, Chen ZH (2008) Study on good agricultural practice for Tulipa edulis-planting density and sowing depth tests. Chin J Chin Mater Med 33:2463–2466 (in Chinese with English abstract)

    Google Scholar 

  • Bock FD, Fer A (1992) Effects of abscisic acid on the transfer of sucrose from host, Pelargonium zonale (L.) Aiton, to a phanerogamic parasite, Cuscuta reflexa Roxb. Aust J Plant Biol 19:679–691

    Article  Google Scholar 

  • Borzenkova RA, Sobyanina EA, Pozdeeva AA, Yashkov MY (1998) Effect of phytohormones on starch-synthesizing capacity in growing potato tubers. Russ J Plant Physiol 45:472–480

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and senstitive method for the quantication of microgram quantities of protein by utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Burton WG, van Es A, Hartmans KJ (1992) The physics and physiology of storage. Potato Crop 2:608–727

    Article  Google Scholar 

  • Cheng L, Li S, Xu X, Hussain J, Yin J, Zhang Y, Li L, Chen X (2013b) Identification of differentially expressed genes relevant to corm formation in Sagittaria trifolia. Plos One 8:e54573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng L, Li S, Yin J, Li L, Chen X (2013a) Genome-wide analysis of differentially expressed genes relevant to rhizome formation in lotus root (Nelumbo nucifera Gaertn). Plos One 8:e67116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chinese Herbalism Editorial Board (1999) Chinese Materia Medica, Shanghai Science and Technology Press, Shanghai, pp 7228–7229

    Google Scholar 

  • Chope GA, Cools K, Hammond JP, Thompson AJ, Terry LA (2012) Physiological, biochemical and transcriptional analysis of onion bulbs during storage. Ann Bot 109:819–831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chow YN, Selby C, Harvey BMR (1992) Stimulation by sucrose of Narcissus bulbil formation in vitro. J Hortic Sci 67:289–293

    Article  CAS  Google Scholar 

  • D’Aoust MA, Yelle S, Nguyen-Quoc B (1999) Antisense inhibition of tomato fruit sucrose synthase decreases fruit setting and the sucrose unloading capacity of young fruit. Plant Cell 11:2407–2418

    Article  PubMed  PubMed Central  Google Scholar 

  • Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63:3367–3377

    Article  CAS  PubMed  Google Scholar 

  • Fernie AR, Willmitzer L, Trethewey RN (2002) Sucrose to starch: a transition in molecular plant physiology. Trends Plant Sci 7:35–41

    Article  CAS  PubMed  Google Scholar 

  • Fernie AR, Willmitzer L (2001) Molecular and biochemical triggers of potato tuber development. Plant Physiol 127:1459–1465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Firon N, LaBonte D, Villordon A, Kfir Y, Solis J, Lapis E, Perlman TS, Doron-Faigenboim A, Hetzroni A, Althan L, Nadir LA (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 Genomics 14:460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gamez-Arjona FM, Li J, Raynaud S, Baroja-Fernández E, Muñoz FJ, Ovecka M, Ragel P, Bahaji A, Pozueta-Romero J, Mérida Á (2011) Enhancing the expression of starch synthase class IV results in increased levels of both transitory and long-term storage starch. Plant Biotechnol J 9:1049–1060

    Article  CAS  PubMed  Google Scholar 

  • García MNM, Stritzler M, Capiati DA (2014) Heterologous expression of Arabidopsis ABF4 gene in potato enhances tuberization through ABA-GA crosstalk regulation. Planta 239:615–631

    Article  Google Scholar 

  • Geigenberger P (2003) Regulation of sucrose to starch conversion in growing potato tubers. J Exp Bot 54:457–465

    Article  CAS  PubMed  Google Scholar 

  • Geigenberger P, Merlo L, Reimholz R, Stitt M (1994) When growing potato tubers are detached from their mother plant there is a rapid inhibition of starch synthesis, involving inhibition of adpglucose pyrophosphorylase. Planta 193:486–493

    Article  CAS  Google Scholar 

  • Hannapel DJ (1991) Characterization of the early events of potato tuber development. Physiol Plantarum 83:568–573

    Article  CAS  Google Scholar 

  • He Z (1993) A Laboratory Guide to Chemical Control Technology on Field Crop, Beijing Agricultural University Press, Beijing, China, pp 60–68

    Google Scholar 

  • Hu F, Wang D, Zhao X, Zhang T, Sun H, Zhu L, Zhang F, Li L, Li Q, Tao D, Fu B, Li Z. (2011) Identification of rhizome-specific genes by genome-wide differential expression analysis in Oryza longistaminata. BMC Plant Biol 11:18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Annu Rev Plant Biol 47:431–444

    Article  CAS  Google Scholar 

  • Husen A, Pal M (2007) Metabolic changes during adventitious root primordium development in Tectona grandis Linn. f. (teak) cuttings as affected by age of donor plants and auxin (IBA and NAA) treatment. New Forest 33:309–323

    Article  Google Scholar 

  • Ishimori T, Niimi Y, Han DS (2007) Benzyladenine and low temperature promote phase transition from juvenile to vegetative adult in bulblets of Lilium× formolongi ‘White Aga’cultured in vitro. Plant Cell Tiss Org 88:313–318

    Article  CAS  Google Scholar 

  • Jackson SD (1999) Multiple signaling pathways control tuber nduction in potato. Plant Physiol 119:1–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaminski KP, Petersen AH, Sønderkær M, Pedersen LH, Pedersen H, Feder C, Nielsen KL (2012) Transcriptome analysis suggests that starch synthesis may proceed via multiple metabolic routes in high yielding potato cultivars. Plos One 7:e51248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karppinen K, Hirvelä E, Nevala T, Sipari N, Suokas M, Jaakola L (2013) Changes in the abscisic acid levels and related gene expression during fruit development and ripening in bilberry (Vaccinium myrtillus L.). Phytochemistry 95:127–134

    Article  CAS  PubMed  Google Scholar 

  • Kim KJ, Kim KS (2005) Changes of endogenous growth substances during bulb maturation after flowering in Lilium oriental hybrid ‘Casa Blanca’. Acta Hortic 570:661–667

    Article  Google Scholar 

  • Kim SK, Son TK, Park SY, Lee IJ, Lee BH, Kim HY, Lee SC (2006) Influences of gibberellin and auxin on endogenous plant hormone and starch mobilization during rice seed germination under salt stress. J Environ Biol 27:181–186

    CAS  Google Scholar 

  • Kloosterman B, De Koeyer D, Griffiths R, Flinn B, Steuernagel B, Scholz U, Sonnewald S, Sonnewald U, Bryan GJ, Prat S, Bánfalvi Z, Hammond JP, Geigenberger P, Nielsen KL, Visser RGF, Bachem CWB (2008) Genes driving potato tuber initiation and growth: identification based on transcriptional changes using the POCI array. Funct Integr Genomic 8:329–340

    Article  CAS  Google Scholar 

  • Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246

    Article  CAS  PubMed  Google Scholar 

  • Kolachevskaya OO, Alekseeva VV, Sergeeva LI, Rukavtsova EB, Getman IA, Vreugdenhil D, Buryanov YI, Romanov GA (2015) Expression of auxin synthesis gene tms1 under control of tuberspecific promoter enhances potato tuberization in vitro. J Integr Plant Biol 57:734–744

    Article  CAS  PubMed  Google Scholar 

  • Li K, Okubo H, Matsumoto T (2002) Control of bulb dormancy in hyacinth-a molecular biological approach. Acta Hortic 570:241–245

    Article  CAS  Google Scholar 

  • Li LJ, Xu C, Chen JL, Cao BS (2003) Changes of carbohydrates during lotus rhizome development of Nelumbo nucifera Gaertn. Journal of Yangzhou University, Agricultural and Life Science (in Chinese with English abstract) 24:72–78

    Google Scholar 

  • Li XQ, 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

    Article  CAS  PubMed  Google Scholar 

  • Li X, Wang C, Cheng J, Zhang J, da Silva JA, Liu X, Duan X, Li T, Sun H (2014) Transcriptome analysis of carbohydrate metabolism during bulblet formation and development in Lilium davidii var. unicolor. BMC Plant Biol 14:358

    Article  PubMed  PubMed Central  Google Scholar 

  • Mares DJ, Marscfaner H, Krauss A (1981) Effect of gibberellic acid on growth and carbohydrate metabolism of developing tubers of potato (Solanum tuberosum). Physiol plantarum 52:267–274

    Article  CAS  Google Scholar 

  • Maoelanka M, Bach A (2014) Induction of bulb organogenesis in in vitro cultures of tarda tulip (Tulipa tarda Stapf.) from seedderived explants. In Vitro Cell Dev-Pl 50:712–721

    Article  Google Scholar 

  • Masuda JI, Ozaki Y, Okubo H (2007) Rhizome transition to storage organ is under phytochrome control in lotus (Nelumbo nucifera). Planta 226:909–915

    Article  CAS  PubMed  Google Scholar 

  • Miao YY, Zhu ZB, Guo QS, Ma HL, Zhu LF (2015) Alternate wetting and drying irrigation-mediated changes in the growth, photosynthesis and yield of the medicinal plant Tulipa edulis. Ind Crop Prod 66:81–88

    Article  Google Scholar 

  • Mishra P, Dubey RS (2013) Excess nickel modulates activities of carbohydrate metabolizing enzymes and induces accumulation of sugars by upregulating acid invertase and sucrose synthase in rice seedlings. Biometals 26:97–111

    Article  CAS  PubMed  Google Scholar 

  • Mitprasat M, Roytrakul S, Jiemsup S, Boonseng O, Yokthongwattana K (2011) Leaf proteomic analysis in cassava (Manihot esculenta, Crantz) during plant development, from planting of stem cutting to storage root formation. Planta 233:1209–1221

    Article  CAS  PubMed  Google Scholar 

  • Mukerjea R, Falconer DJ, Yoon SH, Robyt JF (2010) Large-scale isolation, fractionation, and purification of soluble starch-synthesizing enzymes: starch synthase and branching enzyme from potato tubers. Carbohyd Res 345:1555–1563

    Article  CAS  Google Scholar 

  • Nakamura Y, Yuki K, Park SY (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant Cell Physiol 30:833–839

    CAS  Google Scholar 

  • Niu S, Li Z, Yuan H, Fang P, Chen X, Li W (2013) Proper gibberellin localization in vascular tissue is required to regulate adventitious root development in tobacco. J Exp Bot 64:3411–3424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Podwyszyñska M (2006) Improvement of bulb formation in micropropagated tulips by treatment with NAA and paclobutrazol or ancymidol. In V International Symposium on In Vitro Culture and Horticultural Breeding 725:679–684

    Google Scholar 

  • Podwyszyñska M, Ross H (2003) Formation of tulip bulbs in vitro. Acta Hortic 616:413–419

    Article  Google Scholar 

  • Ptak A (2014) Leucojum aestivum L. in vitro bulbs induction and acclimatization. Open Life Sci 9:1011–1021

    CAS  Google Scholar 

  • Ribeiro PR, Fernandez LG, Castro RDD, Ligterink W, Hilhorst HW (2014) Physiological and biochemical responses of Ricinus communis seedlings to different temperatures: a metabolomics approach. BMC Plant Biol 14:223

    Article  PubMed  PubMed Central  Google Scholar 

  • Rice RD, Alderson PG, Wright NA (1983) Induction of bulbing of tulip shoots in vitro. Sci Hortic 20:377–390

    Article  CAS  Google Scholar 

  • Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW (2001) Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling. Plant J 26:421–433

    Article  CAS  PubMed  Google Scholar 

  • Rouhier H, Usuda H (2001) Spatial and temporal distribution of sucrose synthase in the radish hypocotyls in relation to thickening growth. Plant Cell Physiol 42:583–593

    Article  CAS  PubMed  Google Scholar 

  • Roumeliotis E, Kloosterman B, Oortwijn M, Kohlen W, Bouwmeester HJ, Visser RG, Bachem CW (2012) The effects of auxin and strigolactones on tuber initiation and stolon architecture in potato. J Exp Bot 63:4539–4547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkar D (2008) The signal transduction pathways controlling in planta tuberization in potato: an emerging synthesis. Plant Cell Rep 27:1–8

    Article  CAS  PubMed  Google Scholar 

  • Shin KS, Chkerabarty D, Paek KY (2002) Sprouting rate, changes of carbohydrate contents and related enzymes during cold treatment of lily bulblets regenerated in vitro. Sci Hortic 96:195–204

    Article  CAS  Google Scholar 

  • Sonnewald S, Sonnewald U (2014) Regulation of potato tuber sprouting. Planta 239:27–38

    Article  CAS  PubMed  Google Scholar 

  • Sung SJ, Xu DP, Black CC (1989) Identification of actively filling sucrose sinks. Plant Physiol 89:1117–1121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao X, Gu YH, Wang HY, Zheng W, Li X, Zhao CW, Zhang YZ (2012) Digital gene expression analysis based on integrated de novo transcriptome assembly of sweet potato [Ipomoea batatas (L.) Lam.]. Plos One 7:e36234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uranbey S, Ipek A, Caliskan M, Dundar E, Cocu S, Basalma D, Guneylioglu H (2010) In Vitro bulblet induction from bulb scales of endangered ornamental plant Muscari azureum. Biotechnol Biotec Eq 24:1843–1848

    Article  CAS  Google Scholar 

  • Van Aartrijk J, Blom-Barnhoorn GJ (1981) Growth regulator requirements for adventitious regeneration from Lilium bulbscale tissue in vitro, in relation to duration of bulb storage and cultivar. Sci Hortic 14:261–268

    Article  Google Scholar 

  • Vartapetian BB, Jackson MB (1997) Plant adaptations to anaerobic stress. Ann Bot 79:3–20

    Article  CAS  Google Scholar 

  • Verma AK, Agarwal AK, Dubey RS, Solomon S, Singh SB (2012) Sugar partitioning in sprouting lateral bud and shoot development of sugarcane. Plant Physiol Bioch 62:111–115

    Article  Google Scholar 

  • Viola R, Roberts AG, Haupt S, Gazzani S, Hancock RD, Marmiroli N, Machray GC, Oparka KJ (2001) Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13:385–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiler EW, Jourdan PS, Conrad W (1981) Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta 153:561–571

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang JC, Zhang JH, Wang ZQ, Xu GW, Zhu QS (2004) Activities of key enzymes in sucrose-to-starch conversion in wheat grains subjected to water deficit during grain filling. Plant Physiol 135:1621–1629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Chen TT, Wang ZQ, Yang JC, Zhang JH (2010) Involvement of cytokinins in the grain filling of rice under alternate wetting and drying irrigation. J Exp Bot 61:3719–3733

    Article  CAS  PubMed  Google Scholar 

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Miao, Y., Zhu, Z., Guo, Q. et al. Dynamic changes in carbohydrate metabolism and endogenous hormones during Tulipa edulis stolon development into a new bulb. J. Plant Biol. 59, 121–132 (2016). https://doi.org/10.1007/s12374-016-0456-y

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