A Dynamic Model for Phytohormone Control of Rhizome Growth and Development

  • Eric T. McDowell
  • David R. Gang
Part of the Recent Advances in Phytochemistry book series (RAPT, volume 42)


Despite the economic and medicinal importance of plant rhizomes, the biology of rhizomes has received only cursory attention in recent years. We review the existing literature on rhizome growth, development, and function and discuss outstanding questions that may benefit from application of new technologies such as next-generation sequencing, detailed metabolite profiling, and proteomics. In addition, we outline a new model of the environmental and phytohormone control of rhizome apical dominance and shooting and discuss how this model is followed in different rhizomatous species. The relationship between source carbon availability and specific phytohormones with regard to control of apical dominance is discussed.


Gibberellic Acid Apical Dominance Curcuma Longa Zingiber Officinale Rhizome Growth 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by the United States National Science Foundation (grant numbers DBI-0820346 and DBI-0227618 to D.R.G.).


  1. 1.
    Hemminga MA (1998) The root/rhizome system of seagrasses: an asset and a burden. J Sea Res 39:183–196CrossRefGoogle Scholar
  2. 2.
    Johnson DA, Zhang H, Alldredge JR (2006) Spatial pattern of Verticillium wilt in commercial mint fields. Plant Dis 90:789–797CrossRefGoogle Scholar
  3. 3.
    Kondrat’eva VV, Kirichenko EB, Safronova LM, Voronkova TV (2000) Phytohormones of rhizomes of the mint of various geographic origin in annual cycle of its development. Izv Akad Nauk Ser Biol, 563–568Google Scholar
  4. 4.
    Ivany JA (1997) Effect of rhizome depth in soil on emergence and growth of field mint (Mentha arvensis). Weed Technol 11:149–151Google Scholar
  5. 5.
    Croteau R (1991) Metabolism of monoterpenes in mint (Mentha) species. Planta Med 57:S10–S14CrossRefPubMedGoogle Scholar
  6. 6.
    Sergeeva DS, Popovich AL, Chirny AV (1986) Frost-resistance of mint rhizome depending on the variety and hibernation conditions. Fiziologiya I Biokhimiya Kulturnykh Rastenii 18:391–395Google Scholar
  7. 7.
    Asaeda T, Manatunge J, Roberts J, Hai DN (2006) Seasonal dynamics of resource translocation between the aboveground organs and age-specific rhizome segments of Phragmites australis. Environ Exp Bot 57:9–18CrossRefGoogle Scholar
  8. 8.
    Graneli W, Weisner SE, Sytsma MD (1992) Rhizome dynamics and resource storage in Phragmites australis. Wetlands Ecol Manage 1:239–247CrossRefGoogle Scholar
  9. 9.
    Iwasa Y, Cohen D (1998) Optimal growth schedule of a perennial plant. Am Nat 133:480–505CrossRefGoogle Scholar
  10. 10.
    Iwasa Y, Kubo T (1997) Optimal size of storage for recovery after unpredictable disturbances. Evol Ecol 11:41–65CrossRefGoogle Scholar
  11. 11.
    Tal A, Rubin B (2005) Cyperus esculentus L. – A new weed in Israel. Phytoparasitica 33:245–246CrossRefGoogle Scholar
  12. 12.
    Mojzes A, Kalapos T (2008) Leaf gas exchange responses to abrupt changes in light intensity for two invasive and two non-invasive C-4 grass species. Environ Exp Bot 64:232–238CrossRefGoogle Scholar
  13. 13.
    Cudney DW, Elmore CL, Gibeault VA, Reints JS (1997) Common bermudagrass (Cynodon dactylon) management in cool-season turfgrass. Weed Technol 11:478–483Google Scholar
  14. 14.
    Gunes E, Uludag A, Uremis I (2008) Economic impact of johnsongrass (Sorghum halepense [L.] Pers.) in cotton production in Turkey. J Plant Dis Protect 21:515–520Google Scholar
  15. 15.
    Grant DW, Peters DPC, Beck GK, Fraleigh HD (2003) Influence of an exotic species, Acroptilon repens (L.) DC. on seedling emergence and growth of native grasses. Plant Ecol 166:157–166CrossRefGoogle Scholar
  16. 16.
    Daneshgar P, Jose S, Collins A, Ramsey C (2008) Cogongrass (Imperata cylindrica), an alien invasive grass, reduces survival and productivity of an establishing pine forest. Forest Science 54:579–587Google Scholar
  17. 17.
    Evans CW, Moorhead DJ, Bargeron CT, Douce GK (2007) Implementation of control and prevention strategies for managing cogongrass (Imperata cylindrica) by the Georgia Invasive Species Task Force. Nat Areas J 27:226–231CrossRefGoogle Scholar
  18. 18.
    Ma XQ, Gang DR (2006) Metabolic profiling of in vitro micropropagated and conventionally greenhouse grown ginger (Zingiber officinale). Phytochemistry 67:2239–2255CrossRefPubMedGoogle Scholar
  19. 19.
    Ramirez-Ahumada MD, Timmermann BN, Gang DR (2006) Biosynthesis of curcuminoids and gingerols in turmeric (Curcuma longa) and ginger (Zingiber officinale): Identification of curcuminoid synthase and hydroxycinnamoyl-CoA thioesterases. Phytochemistry 67:2017–2029CrossRefGoogle Scholar
  20. 20.
    Dedov VN, Tran VH, Duke CC, Connor M, Christie MJ, Mandadi S, Roufogalis BD (2002) Gingerols: a novel class of vanilloid receptor (VR1) agonists. Br J Pharmacol 137:793–798CrossRefPubMedGoogle Scholar
  21. 21.
    Ficker C, Smith ML, Akpagana K, Gbeassor M, Zhang J, Durst T, Assabgui R, Arnason JT (2003) Bioassay-guided isolation and identification of antifungal compounds from ginger. Phytother Res 17:897–902CrossRefPubMedGoogle Scholar
  22. 22.
    Jayaprakasha GK, Jagan L, Rao M, Sakariah KK (2005) Chemistry and biological activities of C. longa. Trends Food Sci Technol 16:533–548CrossRefGoogle Scholar
  23. 23.
    Park M, Bae J, Lee DS (2008) Antibacterial activity of [10]-gingerol and [12]-gingerol isolated from ginger rhizome against periodontal bacteria. Phytother Res 22:1446–1449CrossRefPubMedGoogle Scholar
  24. 24.
    Brown AC, Shah C, Liu J, Pham JTH, Zhang JG, Jadus MR (2009) Ginger’s (Zingiber officinale Roscoe) inhibition of rat colonic adenocarcinoma cells proliferation and angiogenesis in vitro. Phytother Res 23:640–645CrossRefPubMedGoogle Scholar
  25. 25.
    Jung HA, Yoon NY, Bae HJ, Min BS, Choi JS (2008) Inhibitory activities of the alkaloids from Coptidis rhizoma against aldose reductase. Arch Pharm Res 31:1405–1412CrossRefPubMedGoogle Scholar
  26. 26.
    Kandhasamy M, Arunachalam KD, Thatheyus AJ (2008) Drynaria quercifolia (L.) J. Sm: a potential resource for antibacterial activity. Afr J Microbiol Res 2:202–205Google Scholar
  27. 27.
    Mukherjee PK, Mukherjee D, Maji AK, Rai S, Heinrich M (2009) The sacred lotus (Nelumbo nucifera) – phytochemical and therapeutic profile. J Pharm Pharmacol 61:407–422PubMedGoogle Scholar
  28. 28.
    Policegoudra RS, Kumar MHS, Aradhya MS (2007) Accumulation of bioactive compounds during growth and development of mango ginger (Curcuma amada Roxb.) rhizomes. J Agric Food Chem 55:8105–8111CrossRefPubMedGoogle Scholar
  29. 29.
    Yamasaki K (2000) Bioactive saponins in Vietnamese ginseng, Panax vietnamensis. Pharm Biol 38:16–24CrossRefGoogle Scholar
  30. 30.
    Akamine H, Hossain MA, Ishimine Y, Kuramochi H (2007) Bud sprouting of torpedograss (Panicum repens L.) as influenced by the rhizome moisture content. Weed Biol Manage 7:188–191CrossRefGoogle Scholar
  31. 31.
    Meyer R, Buchhotlz K (1963) Effect of chemicals on buds of quackgrass rhizomes. Weeds 11:4–7CrossRefGoogle Scholar
  32. 32.
    Hull R (1970) Germination control of Johnsongrass rhizome buds. Weeds 18:118–121Google Scholar
  33. 33.
    McIntyre G (1964) Influence of nitrogen nutrition on bud and rhizome development in Agropyron repens L. Beauv. Nature 203:1084–1085CrossRefGoogle Scholar
  34. 34.
    McIntyre G (1970) Studies on bud development in the rhizome of Agropyron repens. 1. The influence of temperature, light intensity, and bud position on the pattern of development. Can J Bot 48:1903–1909CrossRefGoogle Scholar
  35. 35.
    McIntyre G (1971) Apical dominance in the rhizome of Agropyron repens. Some factors affecting the degree of dominance in isolated rhizomes. Can J Bot 49:99–109CrossRefGoogle Scholar
  36. 36.
    Palmer J (1962) Studies in the behaviour of the rhizome of Agropyron repens (L.) Beauv. II. effect of soil factors on the orientation of the rhizome. Physiol Plant 15:445–451CrossRefGoogle Scholar
  37. 37.
    Ware S (1972) Growth and dormancy in Talinum rhizomes. Ecology 53:1195–1199CrossRefGoogle Scholar
  38. 38.
    Hudson ME (2008) Sequencing breakthroughs for genomic ecology and evolutionary biology. Mol Ecol Resour 8:3–17CrossRefPubMedGoogle Scholar
  39. 39.
    Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen ZT, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu PG, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedGoogle Scholar
  40. 40.
    Dolan L (2009) Body building on land – morphological evolution of land plants. Curr Opin Plant Biol 12:4–8CrossRefPubMedGoogle Scholar
  41. 41.
    Niklas KJ, Kutschera U (2009) The evolutionary development of plant body plans. Funct Plant Biol 36:682–695CrossRefGoogle Scholar
  42. 42.
    Langdale JA (2008) Evolution of developmental mechanisms in plants. Curr Opin Genet Dev 18:368–373CrossRefPubMedGoogle Scholar
  43. 43.
    Hueber FM (1961) Hepaticites devonicus: a new fossil liverwort from the Devonian of New York. Ann Mo Bot Gard 48:125–132CrossRefGoogle Scholar
  44. 44.
    Karssilov V, Schuster R (1984) Paleozoic and mesozoic fossils. In: Schuster RM (ed) New manual of bryology. The Hattori Botanical Garden, Nichinan, pp 1172–1193Google Scholar
  45. 45.
    Malcolm B, Malcolm N (2000) Mosses and other bryophytes: an illustrated glossary. Micro-Optic PressGoogle Scholar
  46. 46.
    Oostendorp C (1987) The bryophytes of the Paleozoic and Mesozoic. Bryophytorium Bibliotheca 34:112Google Scholar
  47. 47.
    Schuster RM (1966) The Hepaticae and Anthocerotae of North America, east of the hundredth meridian. Columbia University Press, NYGoogle Scholar
  48. 48.
    Hu FY, Tao DY, Sacks E, Fu BY, Xu P, Li J, Yang Y, McNally K, Khush GS, Paterson AH, Li ZK (2003) Convergent evolution of perenniality in rice and sorghum. Proc Natl Acad Sci USA 100:4050–4054CrossRefPubMedGoogle Scholar
  49. 49.
    Raven JA, Edwards D (2001) Roots: evolutionary origins and biogeochemical significance. J Exp Bot 52:381–401, Oxford Univ PressCrossRefPubMedGoogle Scholar
  50. 50.
    Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP, Speck T, Stein WE (1998) Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu Rev Ecol Syst 29:263–292CrossRefGoogle Scholar
  51. 51.
    Ghesquiere A (1985) Evolution of Oryza longistaminata. In: Rice genetics: Proceedings of the international rice genetics symposium. International Rice Research InstituteGoogle Scholar
  52. 52.
    Rasheed MA (2004) Recovery and succession in a multi-species tropical seagrass meadow following experimental disturbance: the role of sexual and asexual reproduction. J Exp Mar Biol Ecol 310:13–45CrossRefGoogle Scholar
  53. 53.
    Olesen B, Marba N, Duarte CM, Savela RS, Fortes MD (2004) Recolonization dynamics in a mixed seagrass meadow: the role of clonal versus sexual processes. Estuaries 27:770–780CrossRefGoogle Scholar
  54. 54.
    Barney JN, Whitlow TH, DiTommaso A (2009) Evolution of an invasive phenotype: shift to belowground dominance and enhanced competitive ability in the introduced range. Plant Ecol 202:275–284CrossRefGoogle Scholar
  55. 55.
    Brooker RW, Callaghan TV, Jonasson S (1999) Nitrogen uptake by rhizomes of the clonal sedge Carex bigelowii: a previously overlooked nutritional benefit of rhizomatous growth. New Phytol 142:35–48CrossRefGoogle Scholar
  56. 56.
    Muir AN (1995) The cost of reproduction to the clonal herb Asarum canadense (wild ginger). Can J Bot-Rev Can Bot 73:1683–1686CrossRefGoogle Scholar
  57. 57.
    Calvo S, Lovison G, Pirrotta M, Di Maida G, Tomasello A, Sciandra M (2006) Modelling the relationship between sexual reproduction and rhizome growth in Posidonia oceanica (L.) Delile. Mar Ecol 27:361–371CrossRefGoogle Scholar
  58. 58.
    Reekie EG (1991) Cost of seed versus rhizome production in Agropyron-repens. Can J Bot-Rev Can Bot 69:2678–2683CrossRefGoogle Scholar
  59. 59.
    Westerbergh A, Doebley J (2004) Quantitative trait loci controlling phenotypes related to the perennial versus annual habit in wild relatives of maize. Theor Appl Genet 109:1544–1553CrossRefPubMedGoogle Scholar
  60. 60.
    Jang CS, Kamps TL, Skinner DN, Schulze SR, Vencill WK, Paterson AH (2006) Functional classification, genomic organization, putatively cis-acting regulatory elements, and relationship to quantitative trait loci, of sorghum genes with rhizome-enriched expression. Plant Physiol 142:1148–1159CrossRefPubMedGoogle Scholar
  61. 61.
    Wu X, Larson S, Hu Z, Palazzo A, Jones T, Wang R, Jensen K, Chatterton N (2003) Molecular genetic linkage maps for allotetraploid Leymus wildryes (Gramineae: Triticeae). Genome 46:627–646CrossRefPubMedGoogle Scholar
  62. 62.
    Wang K, Peng H, Lin E, Jin Q, Hua X, Yao S, Bian H, Han N, Pan J, Wang J, Deng M, Zhu M (2005) Identification of genes related to the development of bamboo rhizome bud. J Exp Bot 61:551–561CrossRefGoogle Scholar
  63. 63.
    Kaur P, Larson SR, Bushman BS, Wang RRC, Mott IW, Hole D, Thimmapuram J, Gong G, Liu L (2008) Genes controlling plant growth habit in Leymus (Triticeae): maize barren stalk1 (ba1), rice lax panicle, and wheat tiller inhibition (tin3) genes as possible candidates. Funct Integr Genomics 8:375–386CrossRefPubMedGoogle Scholar
  64. 64.
    Shen-Miller J (2002) Sacred lotus, the long-living fruits of China Antique. Seed Sci Res 12:131–143CrossRefGoogle Scholar
  65. 65.
    Hu F-Y, Tao D-Y, Xu P, Li J, Yang Y, Sacks E, McNally K, Cruz TS, Zhou J, Li Z (2001) Two dominant complementary genes controlling rhizomatous expression in Oryza longistaminata. Rice Genet Newslett 18:34–36Google Scholar
  66. 66.
    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 11:18CrossRefPubMedGoogle Scholar
  67. 67.
    Ghesquiere A, Causse M (1992) Linkage study between molecular markers and genes controlling the reproductive barrier in interspecific backcross between O. sativa and O. longistaminata. Rice Genet Newslett 9:28–31Google Scholar
  68. 68.
    Maekawa M, Inukai T, Rikiishi K, Matsuura T, Govidaraj KG (1998) Inheritance of the rhizomatous traits in hybrid of Oryza longistaminata Chev. et Roehr. and O. sativa L. SABRAO J Breeding Genet 30:69–72Google Scholar
  69. 69.
    Jang CS, Kamps TL, Tang H, Bowers JE, Lemke C, Paterson AH (2009) Evolutionary fate of rhizome-specific genes in a non-rhizomatous Sorghum genotype. Heredity 102:266–273CrossRefPubMedGoogle Scholar
  70. 70.
    Chancellor R (1974) The development of dominance amongst shoots arising from fragments of Agropyron repens rhizomes. Weed Res 14:29–38CrossRefGoogle Scholar
  71. 71.
    Pearce D, Taylor J, Robertson J, Harker K, Daly E (1995) Changes in abscisic acid and indole-3-acetic acid in axillary buds of Elytrigia repens released from apical dominance. Physiol Plant 94:110–116CrossRefGoogle Scholar
  72. 72.
    Robertson J, Taylor J, Harker K, Pocock R, Yeung E (1989) Apical dominance in rhizomes of quackgrass (Elytrigia repens): inhibitory effect of scale leaves. Weeds 37:680–687Google Scholar
  73. 73.
    Taylor J, Robertson J, Harker K, Bhalla M, Daly E (1995) Apical dominance in rhizomes of quackgrass, Elytrigia repens: the effect of auxin, cytokinins, and abscisic acid. Can J Bot 73:307–314CrossRefGoogle Scholar
  74. 74.
    McIntyre G (1976) Apical dominance in the rhizome of Agropyron repens: the influence of water stress on bud activity. Can J Bot 54:2747–2754CrossRefGoogle Scholar
  75. 75.
    McIntyre G (1965) Some effects of the nitrogen supply on the growth and development of Agropyron repens L. Beauv. Weed Res 5:1–12CrossRefGoogle Scholar
  76. 76.
    McIntyre G (1987) Studies on the growth and development of Agropyron repens: interacting effects of humidity, calcium, and nitrogen on growth of the rhizome apex and lateral buds. Can J Bot 65:1427–1432CrossRefGoogle Scholar
  77. 77.
    McIntyre G (1967) Environmental control of bud and rhizome development in the seedling of Agropyron repens L. Beauv. Can J Bot 45:1315–1326CrossRefGoogle Scholar
  78. 78.
    McIntyre GI (2001) Control of plant development by limiting factors: a nutritional perspective. Physiol Plant 113:165–175CrossRefPubMedGoogle Scholar
  79. 79.
    McIntyre GC, Cessna AJ (1998) Studies on the growth and development of the rhizome and lateral rhizome buds in Elytrigia repens: some effects of parent shoot excision. Can J Bot 76:769–776Google Scholar
  80. 80.
    McIntyre G (1969) Apical dominance in the rhizome of Agropyron repens. Evidence of competition for carbohydrate as a factor in the mechanism of inhibition. Can J Bot 47:1189–1197CrossRefGoogle Scholar
  81. 81.
    Wells W, Riopel J (1972) In vitro studies of adventitious rooting in Convolvulus sepium L. Bot Gaz 133:325–330CrossRefGoogle Scholar
  82. 82.
    Chao WS, Serpe MD, Anderson JV, Gesch RW, Horvath DP (2006) Sugars, hormones, and environment affect the dormancy status in underground adventitious buds of leafy spurge (Euphorbia esula). Weed Sci 54:59–68CrossRefGoogle Scholar
  83. 83.
    Chatfield S, Stirnberg P, Forde B, Leyser O (2000) The hormonal regulation of axillary bud growth in Arabidopsis. Plant J 24:159–169CrossRefPubMedGoogle Scholar
  84. 84.
    Leakey R, Chancellor R (1975) Parental factors in dominance of lateral buds on rhizomes of Agropyron repens (L.) Beauv. Planta 123:267–274CrossRefGoogle Scholar
  85. 85.
    Rogan PG, Smith DL (1976) Experimental control of bud inhibition in rhizomes of Agropyron repens (L.) Beauv. Zeitschrift Fur Pflanzenphysiologie 78:113–121Google Scholar
  86. 86.
    Fisher J, Burg S, Kang B (1974) Relationship of auxin transport to branch dimorphism in Cordyline, a woody monocotyledon. Plant Physiol 31:284–287CrossRefGoogle Scholar
  87. 87.
    de Almeida J, Kascheres C, Pereira M (2005) Ethylene and abscisic acid in the control of development of the rhizome of Kohleria eriantha (Benth.) Hanst. (Gesneriaceae). Brazilian J Plant Physiol 17:391–399Google Scholar
  88. 88.
    Brady SM, Sarkar SF, Bonetta D, McCourt P (2003) The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J 34:67–75CrossRefPubMedGoogle Scholar
  89. 89.
    Cline MG, Oh C (2006) A reappraisal of the role of abscisic acid and its interaction with auxin in apical dominance. Ann Bot 98:891–897CrossRefPubMedGoogle Scholar
  90. 90.
    De Smet I, Signora L, Beeckman T, Inze D, Foyer CH, Zhang HM (2003) An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J 33:543–555CrossRefPubMedGoogle Scholar
  91. 91.
    De Smet I, Zhang HM, Inze D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439CrossRefPubMedGoogle Scholar
  92. 92.
    Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17CrossRefPubMedGoogle Scholar
  93. 93.
    Benschop JJ, Millenaar FF, Smeets ME, van Zanten M, Voesenek L, Peeters AJM (2007) Abscisic acid antagonizes ethylene-induced hyponastic growth in Arabidopsis. Plant Physiol 143:1013–1023CrossRefPubMedGoogle Scholar
  94. 94.
    Chiwocha SDS, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross ARS, Kermode AR (2005) The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J 42:35–48CrossRefPubMedGoogle Scholar
  95. 95.
    Grossmann K, Hansen H (2001) Ethylene-triggered abscisic acid: a principle in plant growth regulation? Physiol Plant 113:9–14CrossRefGoogle Scholar
  96. 96.
    Hansen H, Grossmann K (2000) Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiol 124:1437–1448CrossRefPubMedGoogle Scholar
  97. 97.
    Kende H, Zeevaart JAD (1997) The five “classical” plant hormones. Plant Cell 9:1197–1210CrossRefPubMedGoogle Scholar
  98. 98.
    Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. J Exp Bot 53:33–37CrossRefPubMedGoogle Scholar
  99. 99.
    Achard P, Cheng H, Grauwe LD, Decat J, Schoutteten H, Moritz T, Straeten DVD, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94CrossRefPubMedGoogle Scholar
  100. 100.
    Domagalska MA, Sarnowska E, Nagy F, Davis SJ (2010) Genetic analyses of interactions among gibberellin, abscisic acid, and brassinosteroids in the control of flowering time in Arabidopsis thaliana. PLoS One 5:e14012CrossRefPubMedGoogle Scholar
  101. 101.
    Ogura-Tsujita Y, Okubo H (2006) Effect of low nitrogen medium on endogenous changes in ethylene, auxins, and cytokinins in in vitro shoot formation from rhizomes of Cymbidium kanran. In Vitro Cell Dev Biol Plant 42:614–616CrossRefGoogle Scholar
  102. 102.
    Shimasaki K (1995) Interactive effects between cytokinin and ethephon on shoot formation in rhizome cultures of Cymbidium kanran Makino. Plant Tissue Cult Lett 12:27–33CrossRefGoogle Scholar
  103. 103.
    Chen C, Ertl J, Leusner S, Chang C (1985) Localization of cytokinin biosynthetic sites in pea plants and carrot roots. Plant Physiol 78:510–513CrossRefPubMedGoogle Scholar
  104. 104.
    Nordstrom A, Tarkowski P, Tarkowska D, Norbaek R, Åstot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: A factor of potential importance for auxin–cytokinin-regulated development. Proc Natl Acad Sci USA 101:8039–8044CrossRefPubMedGoogle Scholar
  105. 105.
    Tanaka M, Takei K, Kojima M, Sakakibara H, Mori H (2006) Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J 45:1028–1036CrossRefPubMedGoogle Scholar
  106. 106.
    Werner T, Kollmer I, Bartrina I, Holst K, Schmulling T (2006) New insights into the biology of cytokinin degradation. Plant Biol 8:371–381CrossRefPubMedGoogle Scholar
  107. 107.
    Shimizu-Sato S, Tanaka M, Mori H (2009) Auxin-cytokinin interactions in the control of shoot branching. Plant Mol Biol 69:429–435CrossRefPubMedGoogle Scholar
  108. 108.
    Bangerth F (1994) Response of cytokinin concentration in the xylem exudate of bean (Phaseolus vulgaris L.) plants to decapitation and auxin treatment, and relationship to apical dominance. Planta 194:439–442CrossRefGoogle Scholar
  109. 109.
    Foo E, Morris SE, Parmenter K, Young N, Wang HT, Jones A, Rameau C, Turnbull CGN, Beveridge CA (2007) Feedback regulation of xylem cytokinin content is conserved in pea and arabidopsis. Plant Physiol 143:1418–1428CrossRefPubMedGoogle Scholar
  110. 110.
    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 108:435–443CrossRefGoogle Scholar
  111. 111.
    Koch EW, Durako MJ (1991) In vitro studies if the submerged angiosperm Ruppia maritima: auxin and cytokinin effects on plant growth and development. Mar Biol 110:1–6CrossRefGoogle Scholar
  112. 112.
    Gail PA (1969) Germination and dormancy breaking requirements for seeds and rhizome buds of Lysimachia quadrifolia L. Bull New Jersey Acad Sci 14:65Google Scholar
  113. 113.
    Leakey RRB, Chancellor RJ, Vinceprue D (1977) Regeneration from rhizome fragments of Agropyron repens. 2. Breaking of late spring dormancy and influence of chilling and node position on growth from single-node fragments. Ann Appl Biol 87:433–441CrossRefGoogle Scholar
  114. 114.
    Metzger J (1985) Role of gibberellins in the environmental control of stem growth in Thlaspi arvensi L. Plant Physiol 78:8–13CrossRefPubMedGoogle Scholar
  115. 115.
    Metzger J (1990) Comparison of biological activities of gibberellins and gibberellin-precursors native to Thlaspi arvensi L. Plant Physiol 94:151–156CrossRefPubMedGoogle Scholar
  116. 116.
    Horvath DP (1999) Role of mature leaves in inhibition of root bud growth in Euphorbia esula L. Weed Sci 47:544–550Google Scholar
  117. 117.
    McKinless J, Alderson PG (1993) Promotion of root emergence in vitro from rhizome buds of Lapageria rosea cv. Nashcourt after proliferation in the presence of paclobutrazol. Plant Cell Tissue Organ Cult 35:115–120CrossRefGoogle Scholar
  118. 118.
    Montaldi E (1969) Gibberellin-sugar interaction regulating the growth habit of bermudagrass (Cynodon dactylon (L) Pers.). Experientia 25:91–92CrossRefPubMedGoogle Scholar
  119. 119.
    Leakey RRB, Chancellor RJ, Vinceprue D (1978) Regeneration from rhizome fragments of Agropyron-repens (L.) Beauv. 4. Effects of light on bud dormancy and development of dominance amongst shoots on multi-node fragments. Ann Bot 42:205–212Google Scholar
  120. 120.
    Koo H, McDowell E, Ma X, Greer K, Kapteyn J, Xie Z, Kim H, Yu Y, Kudrna D, Wing R, Soderlund C, Gang D (2011) Ginger and turmeric expressed sequence tags identify signature genes for rhizome identity and development and the biosynthesis of curcuminoids and gingerols. BMC BiolGoogle Scholar
  121. 120.
    Pratt LH, Liang C, Shah M, Sun F, Wang HM, Reid SP, Gingle AR, Paterson AH, Wing R, Dean R, Klein R, Nguyen HT, Ma HM, Zhao X, Morishige DT, Mullet JE, Cordonnier-Pratt MM (2005) Sorghum expressed sequence tags identify signature genes for drought, pathogenesis, and skotomorphogenesis from a milestone set of 16,801 unique transcripts. Plant Physiol 139:869–884CrossRefPubMedGoogle Scholar
  122. 121.
    Bushman BS, Larson SR, Mott IW, Cliften PF, Wang RRC, Chatterton NJ, Hernandez AG, Ali S, Kim RW, Thimmapuram J, Gong G, Liu L, Mikel MA (2008) Development and annotation of perennial Triticeae ESTs and SSR markers. Genome 51:779–788CrossRefPubMedGoogle Scholar
  123. 122.
    Larson SR, Mayland HF (2007) Comparative mapping of fiber, protein, and mineral content QTLs in two interspecific Leymus wildrye full-sib families. Mol Breed 20:331–347CrossRefGoogle Scholar
  124. 123.
    Cui HC, Benfey PN (2009) Interplay between SCARECROW, GA and LIKE HETEROCHROMATIN PROTEIN 1 in ground tissue patterning in the Arabidopsis root. Plant J 58:1016–1027CrossRefPubMedGoogle Scholar
  125. 124.
    Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119CrossRefPubMedGoogle Scholar
  126. 125.
    Binns AN, Maravolo NC (1972) Apical dominance, polarity, and adventitious growth in Marchantia polymorpha. Am J Bot 59:692–696CrossRefGoogle Scholar
  127. 126.
    Masuda J, Yukio Ozaki Y, Okubo H (2007) Rhizome transition to storage organ is under phytochrome control in lotus (Nelumbo nucifera). Planta 226:909–915CrossRefPubMedGoogle Scholar
  128. 127.
    Li L, Pan E, Xu C, Ye Z, Cao B (2008) Relationship of endogenous hormones, polyamines and salicylic acid contents with rhizome enlargement of Lotus (Nelumbo nucifera Gaertn). Acta Horticulturae 774:67–74Google Scholar
  129. 128.
    Fisher J (1972) Control of shoot-rhizome dimorphism in the woody monocotyledon, Cordyline (Agavaceae). Am J Bot 59:1000–1010CrossRefGoogle Scholar
  130. 129.
    Munoz J (1995) Effects of some plant growth regulators on the growth of the seagrass Cymodocea nodosa (Ucria) Ascherson. Aquatic Bot 51:311–318CrossRefGoogle Scholar
  131. 130.
    Ball NG (1953) The effects of certain growth-regulating substances on the rhizomes of Aegopodium podagraria. J Exp Bot 4:349–362CrossRefGoogle Scholar
  132. 131.
    McIntyre G (1987) Apical dominance in the rhizome of Agropyron repens. Some factors affecting the degree of dominance in isolated rhizomes. Can J Bot 65Google Scholar
  133. 132.
    Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260CrossRefPubMedGoogle Scholar
  134. 133.
    Cornish KZ, Zeevaart JA (1985) Movement of abscisic acid into the apoplast in response to water stress in Xanthium strumarium L. Plant Physiol 78:623–626CrossRefPubMedGoogle Scholar
  135. 134.
    Takei K, Yamaya T, Sakakibara H (2004) Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-Zeatin. J Biol Chem 279:41866–41872CrossRefPubMedGoogle Scholar
  136. 135.
    Wang RC, Tischner R, Gutierrez RA, Hoffman M, Xing XJ, Chen MS, Coruzzi G, Crawford NM (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136:2512–2522CrossRefPubMedGoogle Scholar
  137. 136.
    Dun EA, Hanan J, Beveridge CA (2009) Computational modeling and molecular physiology experiments reveal new insights into shoot branching in pea. Plant Cell 21:3459–3472CrossRefPubMedGoogle Scholar
  138. 137.
    Lin H, Wang RX, Qian Q, Yan MX, Meng XB, Fu ZM, Yan CY, Jiang B, Su Z, Li JY, Wang YH (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525CrossRefPubMedGoogle Scholar
  139. 138.
    Koltai H, Dor E, Hershenhorn J, Joel D, Weininger S, Lekalla S, Shealtiel H, Bhattacharya C, Eliahu E, Resnick N, Barg R, Kapulnik Y (2009) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29:129–136CrossRefGoogle Scholar
  140. 139.
    Ferguson BJ, Beveridge CA (2009) Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol 149:1929–1944CrossRefPubMedGoogle Scholar
  141. 140.
    Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150:482–493CrossRefPubMedGoogle Scholar
  142. 141.
    Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18:2066–2073CrossRefPubMedGoogle Scholar
  143. 142.
    Swarup R, Kargul J, Marchant A, Zadik D, Rahman A, Mills R, Yemm A, May S, Williams L, Millner P, Tsurumi S, Moore I, Napier R, Kerr ID, Bennett MJ (2004) Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell 16:3069–3083CrossRefPubMedGoogle Scholar
  144. 143.
    Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653CrossRefPubMedGoogle Scholar
  145. 144.
    Ottenschlager I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K (2003) Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci USA 100:2987–2991CrossRefPubMedGoogle Scholar
  146. 145.
    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 433:39–44CrossRefPubMedGoogle Scholar
  147. 146.
    Smith V (1992) Gibberellin A1 biosynthesis in Pisum sativum L. II. Biological and biochemical consequences of the le mutation. Plant Physiol 99:372–377CrossRefPubMedGoogle Scholar
  148. 147.
    Sherriff L, McKay M, Ross J, Reid J, Willis C (1994) Decapitation reduces the metabolism of gibberellin A20 to A1 in Pisum sativum L., decreasing the Le/le difference. Plant Physiol 104:227–280Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.School of Plant Sciences and BIO5 InstituteUniversity of ArizonaTucsonUSA
  2. 2.Institute of Biological ChemistryWashington State UniversityPullmanUSA

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