1932

Abstract

Root and tuber crops have been an important part of human nutrition since the early days of humanity, providing us with essential carbohydrates, proteins, and vitamins. Today, they are especially important in tropical and subtropical regions of the world, where they help to feed an ever-growing population. Early induction and storage organ size are important agricultural traits, as they determine yield over time. During potato tuberization, environmental and metabolic status are sensed, ensuring proper timing of tuberization mediated by phloem-mobile signals. Coordinated cellular restructuring and expansion growth, as well as controlled storage metabolism in the tuber, are executed. This review summarizes our current understanding of potato tuber development and highlights similarities and differences to important tuberous root crop species like sweetpotato and cassava. Finally, we point out knowledge gaps that need to be filled before a complete picture of storage organ development can emerge.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-080720-084456
2021-06-17
2024-12-14
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-080720-084456.html?itemId=/content/journals/10.1146/annurev-arplant-080720-084456&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abe M, Kosaka S, Shibuta M, Nagata K, Uemura T et al. 2019. Transient activity of the florigen complex during the floral transition in Arabidopsis thaliana. Development 146:dev171504
    [Google Scholar]
  2. 2. 
    Abelenda JA, Bergonzi S, Oortwijn M, Sonnewald S, Du M et al. 2019. Source-sink regulation is mediated by interaction of an FT homolog with a SWEET protein in potato. Curr. Biol. 29:1178–86.e6The recent finding of potato sugar exporter StSWEET11 and FT ortholog StSP6A interaction provides a possible mechanistic explanation for the observed shift toward symplasmic sucrose unloading in storage organs, which further underlines the important interplay between sugar and FT signaling.
    [Google Scholar]
  3. 3. 
    Abelenda JA, Cruz-Oro E, Franco-Zorrilla JM, Prat S. 2016. Potato StCONSTANS-like1 suppresses storage organ formation by directly activating the FT-like StSP5G repressor. Curr. Biol. 26:872–81
    [Google Scholar]
  4. 4. 
    Abelenda JA, Navarro C, Prat S. 2011. From the model to the crop: genes controlling tuber formation in potato. Curr. Opin. Biotechnol. 22:287–92
    [Google Scholar]
  5. 5. 
    Abelenda JA, Navarro C, Prat S. 2014. Flowering and tuberization: a tale of two nightshades. Trends Plant Sci 19:115–22
    [Google Scholar]
  6. 6. 
    Adeyemo OS, Hyde PT, Setter TL 2019. Identification of FT family genes that respond to photoperiod, temperature and genotype in relation to flowering in cassava (Manihot esculenta, Crantz). Plant Reprod 32:181–91
    [Google Scholar]
  7. 7. 
    Andrés F, Kinoshita A, Kalluri N, Fernández V, Falavigna VS et al. 2020. The sugar transporter SWEET10 acts downstream of FLOWERING LOCUS T during floral transition of Arabidopsis thaliana. BMC Plant Biol 20:53
    [Google Scholar]
  8. 8. 
    Appeldoorn NJG, de Bruijn SM, Koot-Gronsveld EAM, Visser RGF, Vreugdenhil D, van der Plas LHW. 1997. Developmental changes of enzymes involved in conversion of sucrose to hexose-phosphate during early tuberisation of potato. Planta 202:220–26
    [Google Scholar]
  9. 9. 
    Artschwager E. 1924. On the anatomy of the sweet potato root, with notes on internal breakdown. J. Agric. Res. 27:3157–66
    [Google Scholar]
  10. 10. 
    Azeez A, Sane AP. 2015. Photoperiodic growth control in perennial trees. Plant Signal. Behav. 10:e1087631
    [Google Scholar]
  11. 11. 
    Banerjee AK, Chatterjee M, Yu Y, Suh SG, Miller WA, Hannapel DJ. 2006. Dynamics of a mobile RNA of potato involved in a long-distance signaling pathway. Plant Cell 18:3443–57
    [Google Scholar]
  12. 12. 
    Baroja-Fernández E, Muñoz FJ, Montero M, Etxeberria E, Sesma MT et al. 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 50:1651–62
    [Google Scholar]
  13. 13. 
    Batutis EJ, Ewing EE. 1982. Far-red reversal of red light effect during long-night induction of potato (Solanum tuberosum L.) tuberization. Plant Physiol 69:672–74
    [Google Scholar]
  14. 14. 
    Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P. 1993. Physiological signals that induce flowering. Plant Cell 5:1147–55
    [Google Scholar]
  15. 15. 
    Beyene G, Solomon FR, Chauhan RD, Gaitan-Solis E, Narayanan N et al. 2018. Provitamin A biofortification of cassava enhances shelf life but reduces dry matter content of storage roots due to altered carbon partitioning into starch. Plant Biotechnol. J. 16:1186–200
    [Google Scholar]
  16. 16. 
    Bhogale S, Mahajan AS, Natarajan B, Rajabhoj M, Thulasiram HV, Banerjee AK. 2014. MicroRNA156: a potential graft-transmissible microRNA that modulates plant architecture and tuberization in Solanum tuberosum ssp. andigena. Plant Physiol 164:1011–27
    [Google Scholar]
  17. 17. 
    Biemelt S, Tschiersch H, Sonnewald U. 2004. Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135:254–65
    [Google Scholar]
  18. 18. 
    Bishopp A, Help H, El-Showk S, Weijers D, Scheres B et al. 2011. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr. Biol. 21:917–26
    [Google Scholar]
  19. 19. 
    Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R et al. 2005. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17:3257–81
    [Google Scholar]
  20. 20. 
    Bou-Torrent J, Martínez-García JF, García-Martínez JL, Prat S. 2011. Gibberellin A1 metabolism contributes to the control of photoperiod-mediated tuberization in potato. PLOS ONE 6:e24458
    [Google Scholar]
  21. 21. 
    Bürkle L, Hibberd JM, Quick WP, Kühn C, Hirner B, Frommer WB. 1998. The H+-sucrose cotransporter NtSUT1 is essential for sugar export from tobacco leaves. Plant Physiol 118:59–68
    [Google Scholar]
  22. 22. 
    Carrera E, Bou J, García-Martínez JL, Prat S. 2000. Changes in GA 20-oxidase gene expression strongly affect stem length, tuber induction and tuber yield of potato plants. Plant J 22:247–56
    [Google Scholar]
  23. 23. 
    Chailakhyan MK, Yanina LI, Devedzhyan AG, Lotova GN. 1981. Photoperiodism and tuberization with grafting of tobacco on potato. Dokl. Akad. Nauk SSSR 257:1276–80
    [Google Scholar]
  24. 24. 
    Chapin FS III, Schulze E-D, Mooney HA 1990. The ecology and economics of storage in plants. Annu. Rev. Ecol. Evol. Syst. 21:423–47
    [Google Scholar]
  25. 25. 
    Chapman HW. 1958. Tuberization in the potato plant. Physiol. Plant. 11:215–24
    [Google Scholar]
  26. 26. 
    Chaweewan Y, Taylor N. 2015. Anatomical assessment of root formation and tuberization in cassava (Manihot esculenta Crantz). Trop. Plant Biol. 8:1–8
    [Google Scholar]
  27. 27. 
    Chen H, Banerjee AK, Hannapel DJ. 2004. The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J 38:276–84
    [Google Scholar]
  28. 28. 
    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 132:1391–404
    [Google Scholar]
  29. 29. 
    Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S et al. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–11
    [Google Scholar]
  30. 30. 
    Chincinska IA, Liesche J, Krugel U, Michalska J, Geigenberger P et al. 2008. Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol 146:515–28
    [Google Scholar]
  31. 31. 
    Cho L-H, Pasriga R, Yoon J, Jeon J-S, An G 2018. Roles of sugars in controlling flowering time. J. Plant Biol. 61:121–30
    [Google Scholar]
  32. 32. 
    Cho SK, Sharma P, Butler NM, Kang IH, Shah S et al. 2015. Polypyrimidine tract-binding proteins of potato mediate tuberization through an interaction with StBEL5 RNA. J. Exp. Bot. 66:6835–47
    [Google Scholar]
  33. 33. 
    Corbesier L, Bernier G, Périlleux C. 2002. C:N ratio increases in the phloem sap during floral transition of the long-day plants Sinapis alba and Arabidopsis thaliana. Plant Cell Physiol 43:684–88
    [Google Scholar]
  34. 34. 
    Craine JM, Elmore AJ, Wang L, Aranibar J, Bauters M et al. 2018. Isotopic evidence for oligotrophication of terrestrial ecosystems. Nat. Ecol. Evol. 2:1735–44
    [Google Scholar]
  35. 35. 
    Dingkuhn M, Luquet D, Fabre D, Muller B, Yin X, Paul MJ. 2020. The case for improving crop carbon sink strength or plasticity for a CO2-rich future. Curr. Opin. Plant Biol. 56:259–72
    [Google Scholar]
  36. 36. 
    Dong T, Zhu M, Yu J, Han R, Tang C et al. 2019. RNA-Seq and iTRAQ reveal multiple pathways involved in storage root formation and development in sweet potato (Ipomoea batatas L.). BMC Plant Biol 19:136
    [Google Scholar]
  37. 37. 
    Dutt S, Manjul AS, Raigond P, Singh B, Siddappa S et al. 2017. Key players associated with tuberization in potato: potential candidates for genetic engineering. Crit. Rev. Biotechnol. 37:942–57
    [Google Scholar]
  38. 38. 
    Endler A, Meyer S, Schelbert S, Schneider T, Weschke W et al. 2006. Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol 141:196–207
    [Google Scholar]
  39. 39. 
    Eriksson ME, Israelsson M, Olsson O, Moritz T. 2000. Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat. Biotechnol. 18:784–88
    [Google Scholar]
  40. 40. 
    Evans JR. 1989. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19
    [Google Scholar]
  41. 41. 
    Eviatar-Ribak T, Shalit-Kaneh A, Chappell-Maor L, Amsellem Z, Eshed Y, Lifschitz E. 2013. A cytokinin-activating enzyme promotes tuber formation in tomato. Curr. Biol. 23:1057–64
    [Google Scholar]
  42. 42. 
    Ewing EE, Struik PC 1992. Tuber formation in the potato: induction, initiation and growth. Horticultural Reviews, Vol. 14 J Janick 89–198 New York: Wiley
    [Google Scholar]
  43. 43. 
    Fernie AR, Willmitzer L. 2001. Molecular and biochemical triggers of potato tuber development. Plant Physiol 127:1459–65
    [Google Scholar]
  44. 44. 
    Ferreira SJ, Senning M, Sonnewald S, Kessling P-M, Goldstein R, Sonnewald U. 2010. Comparative transcriptome analysis coupled to X-ray CT reveals sucrose supply and growth velocity as major determinants of potato tuber starch biosynthesis. BMC Genom 11:93
    [Google Scholar]
  45. 45. 
    Firon N, LaBonte D, Villordon A, Kfir Y, Solis J 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
    [Google Scholar]
  46. 46. 
    Fischer U, Kucukoglu M, Helariutta Y, Bhalerao RP. 2019. The dynamics of cambial stem cell activity. Annu. Rev. Plant Biol. 70:293–319
    [Google Scholar]
  47. 47. 
    Food Agric. Org. U.N 2018. FAOSTAT Food Agric. Org U.N.: updated March 5, 2020, retrieved May 14, 2020. https://www.fao.org/faostat/en/#data/QC
    [Google Scholar]
  48. 48. 
    Forde BG. 2002. Local and long-range signaling pathways regulating plant responses to nitrate. Annu. Rev. Plant Biol. 53:203–24
    [Google Scholar]
  49. 49. 
    Galvão VC, Fankhauser C. 2015. Sensing the light environment in plants: photoreceptors and early signaling steps. Curr. Opin. Neurobiol. 34:46–53
    [Google Scholar]
  50. 50. 
    Ghate TH, Sharma P, Kondhare KR, Hannapel DJ, Banerjee AK. 2017. The mobile RNAs, StBEL11 and StBEL29, suppress growth of tubers in potato. Plant Mol. Biol. 93:563–78
    [Google Scholar]
  51. 51. 
    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 70:678–90
    [Google Scholar]
  52. 52. 
    Gregory LE. 1956. Some factors for tuberization in the potato plant. Am. J. Bot. 43:281–88
    [Google Scholar]
  53. 53. 
    Gutaker RM, Weiß CL, Ellis D, Anglin NL, Knapp S et al. 2019. The origins and adaptation of European potatoes reconstructed from historical genomes. Nat. Ecol. Evol. 3:1093–101
    [Google Scholar]
  54. 54. 
    Ham B-K, Li G, Kang B-H, Zeng F, Lucas WJ. 2012. Overexpression of Arabidopsis plasmodesmata germin-like proteins disrupts root growth and development. Plant Cell 24:3630–48
    [Google Scholar]
  55. 55. 
    Hannapel DJ, Sharma P, Lin T, Banerjee AK. 2017. The multiple signals that control tuber formation. Plant Physiol 174:845–56
    [Google Scholar]
  56. 56. 
    Hardigan MA, Laimbeer FPE, Newton L, Crisovan E, Hamilton JP et al. 2017. Genome diversity of tuber-bearing Solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato. PNAS 114:E9999–10008
    [Google Scholar]
  57. 57. 
    Harig L, Beinecke FA, Oltmanns J, Muth J, Müller O et al. 2012. Proteins from the FLOWERING LOCUS T-like subclade of the PEBP family act antagonistically to regulate floral initiation in tobacco. Plant J 72:908–21
    [Google Scholar]
  58. 58. 
    Hay A, Tsiantis M. 2010. KNOX genes: versatile regulators of plant development and diversity. Development 137:3153–65
    [Google Scholar]
  59. 59. 
    Howeler R, Lutaladio N, Thomas G. 2013. Save and grow: cassava. A guide to sustainable production intensification Food Agric. Org U.N., Rome:
    [Google Scholar]
  60. 60. 
    Imaizumi T, Kay SA. 2006. Photoperiodic control of flowering: not only by coincidence. Trends Plant Sci 11:550–58
    [Google Scholar]
  61. 61. 
    Immanen J, Nieminen K, Smolander OP, Kojima M, Alonso Serra J et al. 2016. Cytokinin and auxin display distinct but interconnected distribution and signaling profiles to stimulate cambial activity. Curr. Biol. 26:1990–97This paper highlights distinct hormonal gradients and related signaling events across the vascular cambium of Populus trichocarpa with distinct effects on meristematic daughter cell development.
    [Google Scholar]
  62. 62. 
    Jackson SD. 1999. Multiple signaling pathways control tuber induction in potato. Plant Physiol 119:1–8
    [Google Scholar]
  63. 63. 
    Jackson SD. 2009. Plant responses to photoperiod. New Phytol 181:517–31
    [Google Scholar]
  64. 64. 
    Jackson SD, Heyer A, Dietze J, Prat S. 1996. Phytochrome B mediates the photoperiodic control of tuber formation in potato. Plant J 9:159–66
    [Google Scholar]
  65. 65. 
    Jackson SD, James P, Prat S, Thomas B. 1998. Phytochrome B affects the levels of a graft-transmissible signal involved in tuberization. Plant Physiol 117:29–32
    [Google Scholar]
  66. 66. 
    Jang G, Lee JH, Rastogi K, Park S, Oh SH, Lee JY. 2015. Cytokinin-dependent secondary growth determines root biomass in radish (Raphanus sativus L.). J. Exp. Bot. 66:4607–19This paper highlights the importance of cambial cytokinin signaling in radish and its positive influence on root crop yield.
    [Google Scholar]
  67. 67. 
    Jung J-H, Domijan M, Klose C, Biswas S, Ezer D et al. 2016. Phytochromes function as thermosensors in Arabidopsis. Science 354:886–89
    [Google Scholar]
  68. 68. 
    Kloosterman B, Abelenda JA, Gomez MMC, Oortwijn M, de Boer JM et al. 2013. Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature 495:246–50
    [Google Scholar]
  69. 69. 
    Kloosterman B, De Koeyer D, Griffiths R, Flinn B, Steuernagel B et al. 2008. Genes driving potato tuber initiation and growth: identification based on transcriptional changes using the POCI array. Funct. Integr. Genom. 8:329–40
    [Google Scholar]
  70. 70. 
    Kloosterman B, Navarro C, Bijsterbosch G, Lange T, Prat S et al. 2007. StGA2ox1 is induced prior to stolon swelling and controls GA levels during potato tuber development. Plant J 52:362–73
    [Google Scholar]
  71. 71. 
    Kolachevskaya OO, Alekseeva VV, Sergeeva LI, Rukavtsova EB, Getman IA et al. 2015. Expression of auxin synthesis gene tms1 under control of tuber-specific promoter enhances potato tuberization in vitro. J. Integr. Plant Biol. 57:734–44
    [Google Scholar]
  72. 72. 
    Kondhare KR, Natarajan B, Banerjee AK. 2020. Molecular signals that govern tuber development in potato. Int. J. Dev. Biol. 64:133–40
    [Google Scholar]
  73. 73. 
    Kondhare KR, Vetal PV, Kalsi HS, Banerjee AK. 2019. BEL1-like protein (StBEL5) regulates CYCLING DOF FACTOR1 (StCDF1) through tandem TGAC core motifs in potato. J. Plant Physiol. 241:153014
    [Google Scholar]
  74. 74. 
    Krauss A, Marschner H. 1982. Influence of nitrogen nutrition, daylength and temperature on contents of gibberellic and abscisic acid and on tuberization in potato plants. Potato Res 25:13–21
    [Google Scholar]
  75. 75. 
    Kühn C, Hajirezaei M-R, Fernie AR, Roessner-Tunali U, Czechowski T et al. 2003. The sucrose transporter StSUT1 localizes to sieve elements in potato tuber phloem and influences tuber physiology and development. Plant Physiol 131:102–13
    [Google Scholar]
  76. 76. 
    Kumar D, Wareing PF. 1973. Studies on tuberization in Solanum andigena: evidence for the existence and movement of a specific tuberization stimulus. New Phytol 72:283–87
    [Google Scholar]
  77. 77. 
    Lamers J, van der Meer T, Testerink C. 2020. How plants sense and respond to stressful environments. Plant Physiol 182:1624–35
    [Google Scholar]
  78. 78. 
    Lee R, Baldwin S, Kenel F, McCallum J, Macknight R. 2013. FLOWERING LOCUS T genes control onion bulb formation and flowering. Nat. Commun. 4:2884
    [Google Scholar]
  79. 79. 
    Legris M, Klose C, Burgie ES, Rojas CCR, Neme M et al. 2016. Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354:897–900
    [Google Scholar]
  80. 80. 
    Lehretz GG, Sonnewald S, Hornyik C, Corral JM, Sonnewald U. 2019. Post-transcriptional regulation of FLOWERING LOCUS T modulates heat-dependent source-sink development in potato. Curr. Biol. 29:1614–24.e3
    [Google Scholar]
  81. 81. 
    Li X, Zhang D. 2003. Gene expression activity and pathway selection for sucrose metabolism in developing storage root of sweet potato. Plant Cell Physiol 44:630–36
    [Google Scholar]
  82. 82. 
    Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A et al. 2006. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. PNAS 103:6398–403
    [Google Scholar]
  83. 83. 
    Lin T, Sharma P, Gonzalez DH, Viola IL, Hannapel DJ. 2013. The impact of the long-distance transport of a BEL1-like messenger RNA on development. Plant Physiol 161:760–72
    [Google Scholar]
  84. 84. 
    Liu H, Si C, Shi C, Wang S, Sun Z, Shi Y. 2019. Switch from apoplasmic to symplasmic phloem unloading during storage roots formation and bulking of sweetpotato. Crop Sci 59:675–83
    [Google Scholar]
  85. 85. 
    Liu M, Bassetti N, Petrasch S, Zhang N, Bucher J et al. 2019. What makes turnips: anatomy, physiology and transcriptome during early stages of its hypocotyl-tuber development. Hortic. Res. 6:38
    [Google Scholar]
  86. 86. 
    Ma J, Aloni R, Villordon A, Labonte D, Kfir Y et al. 2015. Adventitious root primordia formation and development in stem nodes of ‘Georgia Jet’ sweetpotato, Ipomoea batatas. Am. J. Bot. 102:1040–49
    [Google Scholar]
  87. 87. 
    Mahajan A, Bhogale S, Kang IH, Hannapel DJ, Banerjee AK. 2012. The mRNA of a Knotted1-like transcription factor of potato is phloem mobile. Plant Mol. Biol. 79:595–608
    [Google Scholar]
  88. 88. 
    Martin A, Adam H, Díaz-Mendoza M, Żurczak M, González-Schain ND, Suarez-Lopez P. 2009. Graft-transmissible induction of potato tuberization by the microRNA miR172. Development 136:2873–81
    [Google Scholar]
  89. 89. 
    Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Václavíková K et al. 2008. Cytokinins are central regulators of cambial activity. PNAS 105:20027–31
    [Google Scholar]
  90. 90. 
    Mehdi R, Lamm CE, Bodampalli Anjanappa R, Mudsam C, Saeed M et al. 2019. Symplasmic phloem unloading and radial post-phloem transport via vascular rays in tuberous roots of Manihot esculenta. J. Exp. Bot. 70:5559–73
    [Google Scholar]
  91. 91. 
    Melis RJM, van Staden J. 1985. Tuberization in cassava (Manihot esculenta): cytokinin and abscisic acid activity in tuberous roots. J. Plant Physiol. 118:357–66
    [Google Scholar]
  92. 92. 
    Menzel CM. 1983. Tuberization in potato at high temperatures: gibberellin content and transport from buds. Ann. Bot. 52:697–702
    [Google Scholar]
  93. 93. 
    Miyazawa Y, Sakai A, Miyagishima S, 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 121:461–69
    [Google Scholar]
  94. 94. 
    Morris WL, Hancock RD, Ducreux LJM, Morris JA, Usman M et al. 2014. Day length dependent restructuring of the leaf transcriptome and metabolome in potato genotypes with contrasting tuberization phenotypes. Plant Cell Environ 37:1351–63
    [Google Scholar]
  95. 95. 
    Natarajan B, Kondhare KR, Hannapel DJ, Banerjee AK. 2019. Mobile RNAs and proteins: prospects in storage organ development of tuber and root crops. Plant Sci 284:73–81
    [Google Scholar]
  96. 96. 
    Navarro C, Abelenda JA, Cruz-Oro E, Cuellar CA, Tamaki S et al. 2011. Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478:119–22This paper first identified the potato FT ortholog StSP6A as an important regulator of tuber induction.
    [Google Scholar]
  97. 97. 
    Noh SA, Lee H-S, Huh EJ, Huh GH, Paek KH et al. 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. 61:1337–49One of the few transgenic studies on root crop development outside the potato system. The paper illustrates the importance of early auxin signaling in fibrous root-to-storage root transition in sweetpotato.
    [Google Scholar]
  98. 98. 
    Noh SA, Lee H-S, Huh GH, Oh MJ, Paek KH et al. 2012. A sweetpotato SRD1 promoter confers strong root-, taproot-, and tuber-specific expression in Arabidopsis, carrot, and potato. Transgen. Res. 21:265–78
    [Google Scholar]
  99. 99. 
    Noh SA, Lee H-S, Kim Y-S, Paek K-H, Shin JS, Bae JM. 2012. Down-regulation of the IbEXP1 gene enhanced storage root development in sweetpotato. J. Exp. Bot. 64:129–42
    [Google Scholar]
  100. 100. 
    Odipio J, Beyene G, Chauhan RD, Alicai T, Bart R et al. 2020. Transgenic overexpression of endogenous FLOWERING LOCUS T-like gene MeFT1 produces early flowering in cassava. PLOS ONE 15:e0227199
    [Google Scholar]
  101. 101. 
    Ohto M-A, Onai K, Furukawa Y, Aoki E, Araki T, Nakamura K. 2001. Effects of sugar on vegetative development and floral transition in Arabidopsis. Plant Physiol 127:252–61
    [Google Scholar]
  102. 102. 
    Okazawa Y. 1959. Studies on the occurrence of natural gibberellin and its effects on the tuber formation of potato plants. Jpn. J. Crop Sci. 28:129–33
    [Google Scholar]
  103. 103. 
    Okazawa Y. 1960. Studies on the relation between the tuber formation of potato and its natural gibberellin content. Jpn. J. Crop Sci. 29:121–24
    [Google Scholar]
  104. 104. 
    Okazawa Y, Chapman HW. 1962. Regulation of tuber formation in the potato plant. Physiol. Plant. 15:413–19
    [Google Scholar]
  105. 105. 
    Omondi JO, Lazarovitch N, Rachmilevitch S, Yermiyahu U, Sperling O. 2019. High nitrogen availability limits photosynthesis and compromises carbohydrate allocation to storage in roots of Manihotesculenta Crantz. Front. Plant Sci. 10:1041
    [Google Scholar]
  106. 106. 
    Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T et al. 2010. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330:1397–400
    [Google Scholar]
  107. 107. 
    Pin PA, Nilsson O. 2012. The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ 35:1742–55
    [Google Scholar]
  108. 108. 
    Putterill J, Varkonyi-Gasic E. 2016. FT and florigen long-distance flowering control in plants. Curr. Opin. Plant Biol. 33:77–82
    [Google Scholar]
  109. 109. 
    Ragni L, Greb T. 2018. Secondary growth as a determinant of plant shape and form. Semin. Cell Dev. Biol. 79:58–67
    [Google Scholar]
  110. 110. 
    Rapoport HF, Loomis RS. 1985. Interaction of storage root and shoot in grafted sugar beet and chard. Crop Sci 25:1079–84
    [Google Scholar]
  111. 111. 
    Riesmeier JW, Hirner B, Frommer WB. 1993. Potato sucrose transporter expression in minor veins indicates a role in phloem loading. Plant Cell 5:1591–98
    [Google Scholar]
  112. 112. 
    Riesmeier JW, Willmitzer L, Frommer WB. 1994. Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J 13:1–7
    [Google Scholar]
  113. 112a. 
    Rodrigues CM, Müdsam C, Keller I, Zierer W, Czarnecki Oet al 2020. Vernalization alters sink and source identities and reverses phloem translocation from taproots to shoots in sugar beet. Plant Cell 32:320623
    [Google Scholar]
  114. 113. 
    Rodríguez-Falcón M, Bou J, Prat S. 2006. Seasonal control of tuberization in potato: conserved elements with the flowering response. Annu. Rev. Plant Biol. 57:151–80
    [Google Scholar]
  115. 114. 
    Romanov GA, Aksenova NP, Konstantinova TN, Golyanovskaya SA, Kossman J, Willmitzer L. 2000. Effect of indole-3-acetic acid and kinetin on tuberisation parameters of different cultivars and transgenic lines of potato in vitro. Plant Growth Regul 32:245–51
    [Google Scholar]
  116. 115. 
    Romera-Branchat M, Severing E, Pocard C, Ohr H, Vincent C et al. 2020. Functional divergence of the Arabidopsis florigen-interacting bZIP transcription factors FD and FDP. Cell Rep 31:107717
    [Google Scholar]
  117. 116. 
    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 132:106–17
    [Google Scholar]
  118. 117. 
    Roumeliotis E, Kloosterman B, Oortwijn M, Kohlen W, Bouwmeester HJ et al. 2012. The effects of auxin and strigolactones on tuber initiation and stolon architecture in potato. J. Exp. Bot. 63:4539–47
    [Google Scholar]
  119. 118. 
    Roumeliotis E, Visser RG, Bachem CW. 2012. A crosstalk of auxin and GA during tuber development. Plant Signal. Behav. 7:1360–63
    [Google Scholar]
  120. 119. 
    Ruan Y-L. 2012. Signaling role of sucrose metabolism in development. Mol. Plant 5:763–65
    [Google Scholar]
  121. 119a. 
    Rüscher D, García JMC, Carluccio AV, Klemens PAW, Gisel Aet al 2021. Auxin signaling and vascular cambium formation enables storage metabolism in cassava tuberous roots. J. Exp. Bot In press https://doi.org/10.1093/jxb/erab106
    [Crossref] [Google Scholar]
  122. 120. 
    Schneider S, Hulpke S, Schulz A, Yaron I, Höll J et al. 2012. Vacuoles release sucrose via tonoplast-localised SUC4-type transporters. Plant Biol 14:325–36
    [Google Scholar]
  123. 121. 
    Shalit A, Rozman A, Goldshmidt A, Alvarez JP, Bowman JL et al. 2009. The flowering hormone florigen functions as a general systemic regulator of growth and termination. PNAS 106:8392–97
    [Google Scholar]
  124. 122. 
    Sharma P, Lin T, Hannapel DJ. 2016. Targets of the StBEL5 transcription factor include the FT ortholog StSP6A. Plant Physiol 170:310–24
    [Google Scholar]
  125. 123. 
    Shim JS, Kubota A, Imaizumi T. 2017. Circadian clock and photoperiodic flowering in Arabidopsis: CONSTANS is a hub for signal integration. Plant Physiol 173:5–15
    [Google Scholar]
  126. 124. 
    Singh V, Sergeeva L, Ligterink W, Aloni R, Zemach H et al. 2019. Gibberellin promotes sweetpotato root vascular lignification and reduces storage root formation. Front. Plant Sci. 10:1320
    [Google Scholar]
  127. 125. 
    Smith OE, Rappaport L. 1969. Gibberellins, inhibitors, and tuber formation in the potato, Solanum tuberosum. Am. J. Potato Res. 46:185
    [Google Scholar]
  128. 126. 
    Sojikul P, Saithong T, Kalapanulak S, Pisuttinusart N, Limsirichaikul S et al. 2015. Genome-wide analysis reveals phytohormone action during cassava storage root initiation. Plant Mol. Biol. 88:531–43
    [Google Scholar]
  129. 127. 
    Song YH, Estrada DA, Johnson RS, Kim SK, Lee SY et al. 2014. Distinct roles of FKF1, GIGANTEA, and ZEITLUPE proteins in the regulation of CONSTANS stability in Arabidopsis photoperiodic flowering. PNAS 111:17672–77
    [Google Scholar]
  130. 128. 
    Spooner DM, Núñez J, Trujillo G, del Rosario Herrera M, Guzmán F, Ghislain M 2007. Extensive simple sequence repeat genotyping of potato landraces supports a major reevaluation of their gene pool structure and classification. PNAS 104:19398–403
    [Google Scholar]
  131. 129. 
    Stein O, Granot D. 2019. An overview of sucrose synthases in plants. Front. Plant Sci. 10:95
    [Google Scholar]
  132. 130. 
    Suárez-López P. 2013. A critical appraisal of phloem-mobile signals involved in tuber induction. Front. Plant Sci. 4:253
    [Google Scholar]
  133. 131. 
    Sun J, Wang H, Ren L, Chen S, Chen F, Jiang J 2017. CmFTL2 is involved in the photoperiod- and sucrose-mediated control of flowering time in Chrysanthemum. Hortic. Res. 4:17001
    [Google Scholar]
  134. 132. 
    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. 165:1726–35
    [Google Scholar]
  135. 133. 
    Tao G-Q, Letham DS, Yong JWH, Zhang K, John PCL et al. 2010. Promotion of shoot development and tuberisation in potato by expression of a chimaeric cytokinin synthesis gene at normal and elevated CO2 levels. Funct. Plant Biol. 37:43–54
    [Google Scholar]
  136. 134. 
    Taoka K-I, Ohki I, Tsuji H, Furuita K, Hayashi K et al. 2011. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476:332–35
    [Google Scholar]
  137. 135. 
    Teo CJ, Takahashi K, Shimizu K, Shimamoto K, Taoka KI. 2017. Potato tuber induction is regulated by interactions between components of a tuberigen complex. Plant Cell Physiol 58:365–74The authors first demonstrated that a tuberigen activation complex is formed during potato tuber initiation analog to the florigen activation complex.
    [Google Scholar]
  138. 136. 
    Tsai C-H, Miller A, Martin S, Rodermel S. 1997. Source strength regulates an early phase transition of tobacco shoot morphogenesis. Plant Physiol 115:907–14
    [Google Scholar]
  139. 137. 
    Turck F, Fornara F, Coupland G. 2008. Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59:573–94
    [Google Scholar]
  140. 138. 
    Van Den Berg JH, Šimko I, Davies PJ, Ewing EE, Halinska A. 1995. Morphology and [14C]gibberellin A12 metabolism in wild type and dwarf Solanum tuberosum ssp. andigena grown under long and short photoperiods. J. Plant Physiol. 146:467–73
    [Google Scholar]
  141. 139. 
    Van Harsselaar JK, Lorenz J, Senning M, Sonnewald U, Sonnewald S. 2017. Genome-wide analysis of starch metabolism genes in potato (Solanum tuberosum L.). BMC Genom 18:37
    [Google Scholar]
  142. 140. 
    Viola R, Roberts AG, Haupt S, Gazzani S, Hancock RD et al. 2001. Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13:385–98This paper illustrates the switch from apoplasmic to symplasmic unloading during potato tuber development.
    [Google Scholar]
  143. 141. 
    Vreugdenhil D, Struik PC. 1989. An integrated view of the hormonal regulation of tuber formation in potato (Solanum tuberosum). Physiol. Plant. 75:525–31
    [Google Scholar]
  144. 142. 
    Vulavala VKR, Fogelman E, Faigenboim A, Shoseyov O, Ginzberg I. 2019. The transcriptome of potato tuber phellogen reveals cellular functions of cork cambium and genes involved in periderm formation and maturation. Sci. Rep. 9:10216
    [Google Scholar]
  145. 143. 
    Wang H, Wang H. 2015. The miR156/SPL module, a regulatory hub and versatile toolbox, gears up crops for enhanced agronomic traits. Mol. Plant 8:677–88
    [Google Scholar]
  146. 144. 
    Wang H, Yang J, Zhang M, Fan W, Firon N et al. 2016. Altered phenylpropanoid metabolism in the maize Lc-expressed sweet potato (Ipomoea batatas) affects storage root development. Sci. Rep. 6:18645
    [Google Scholar]
  147. 145. 
    Wang Y, Liu L, Song S, Li Y, Shen L, Yu H. 2017. DOFT and DOFTIP1 affect reproductive development in the orchid Dendrobium Chao Praya Smile. J. Exp. Bot. 68:5759–72
    [Google Scholar]
  148. 146. 
    Wang Z, Fang B, Chen X, Liao M, Chen J et al. 2015. Temporal patterns of gene expression associated with tuberous root formation and development in sweetpotato (Ipomoea batatas). BMC Plant Biol 15:180
    [Google Scholar]
  149. 147. 
    Wang Z, Zhou Z, Liu Y, Liu T, Li Q et al. 2015. Functional evolution of phosphatidylethanolamine binding proteins in soybean and Arabidopsis. Plant Cell 27:323–36
    [Google Scholar]
  150. 148. 
    Wellensiek SJ. 1929. The Physiology of Tuber Formation in Solanum tuberosum L Wageningen, Ger: Meded Landbouwhogesch
    [Google Scholar]
  151. 149. 
    Wigge PA 2011. FT, a mobile developmental signal in plants. Curr. Biol. 21:R374–78
    [Google Scholar]
  152. 150. 
    Wu Y, Shi L, Li L, Fu L, Liu Y et al. 2019. Integration of nutrient, energy, light, and hormone signalling via TOR in plants. J. Exp. Bot. 70:2227–38
    [Google Scholar]
  153. 151. 
    Wuddineh WA, Mazarei M, Zhang J, Poovaiah CR, Mann DG et al. 2015. Identification and overexpression of gibberellin 2-oxidase (GA2ox) in switchgrass (Panicum virgatum L.) for improved plant architecture and reduced biomass recalcitrance. Plant Biotechnol. J. 13:636–47
    [Google Scholar]
  154. 152. 
    Xu L, Wang J, Lei M, Li L, Fu Y et al. 2016. Transcriptome analysis of storage roots and fibrous roots of the traditional medicinal herb Calleryaspeciosa (Champ.) ScHot. PLOS ONE 11:e0160338
    [Google Scholar]
  155. 153. 
    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 117:575–84
    [Google Scholar]
  156. 154. 
    Xu X, Vreugdenhil D, van Lammeren AAM. 1998. Cell division and cell enlargement during potato tuber formation. J. Exp. Bot. 49:573–82This is an excellent paper for readers interested in the anatomy of potato tuber development.
    [Google Scholar]
  157. 155. 
    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
    [Google Scholar]
  158. 156. 
    Yu S, Cao L, Zhou C-M, Zhang T-Q, Lian H et al. 2013. Sugar is an endogenous cue for juvenile-to-adult phase transition in plants. eLife 2:e00269This study identified sugars as the signal that represses mi156 and subsequently triggers the juvenile-to-adult phase transition.
    [Google Scholar]
  159. 157. 
    Yu S, Lian H, Wang J-W. 2015. Plant developmental transitions: the role of microRNAs and sugars. Curr. Opin. Plant Biol. 27:1–7
    [Google Scholar]
  160. 158. 
    Zhang X, Campbell R, Ducreux LJM, Morris J, Hedley PE et al. 2020. TERMINAL FLOWER-1/CENTRORADIALIS inhibits tuberisation via protein interaction with the tuberigen activation complex. Plant J 103:2263–78This recent paper deepens our understanding of the tuberigen activation complex and its regulation.
    [Google Scholar]
  161. 159. 
    Zheng H, Wang Y, Zhao J, Shi X, Ma Z, Fan M 2018. Tuber formation as influenced by the C:N ratio in potato plants. J. Plant. Nutr. Soil Sci. 181:686–93
    [Google Scholar]
  162. 160. 
    Zhou T, Song B, Liu T, Shen Y, Dong L et al. 2019. Phytochrome F plays critical roles in potato photoperiodic tuberization. Plant J 98:42–54
    [Google Scholar]
  163. 161. 
    Zrenner R, Salanoubat M, Willmitzer L, Sonnewald U. 1995. Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J 7:97–107
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-080720-084456
Loading
/content/journals/10.1146/annurev-arplant-080720-084456
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error