Dwarf germplasm: the key to giant Cannabis hempseed and cannabinoid crops

Abstract

After a century of banishment, both euphoric (“marijuana”) and non-euphoric (“industrial hemp”) classes of Cannabis sativa are attracting billions of dollars of investment as new legitimate crops. Most domesticated C. sativa is very tall, a phenotype that is desirable only for hemp fibre obtained from the stems. However, because the principal demands today are for chemicals from the inflorescence and oilseeds from the infructescence, an architecture maximizing reproductive tissues while minimizing stems is appropriate. Such a design was the basis of the greatest short-term increases in crop productivity in the history of agriculture: the creation of short-stature (“semi-dwarf”), high-harvest-index grain cultivars, especially by ideotype breeding, as demonstrated during the “Green Revolution.” This paradigm has considerable promise for C. sativa. The most critical dwarfing character for breeding such productivity into C. sativa is contraction of internodes. This reduces stem tissues (essentially a waste product except for fibre hemp) and results in compact inflorescences (which, on an area basis, maximize cannabinoid chemicals) and infructescences (which maximize oilseed production), as well as contributing to ease of harvesting and efficiency of production on an area basis. Four sources of germplasm useful for breeding semi-dwarf biotypes deserve special attention: (1) Naturally short northern Eurasian wild plants (often photoperiodically day-neutral, unlike like most biotypes) adapted to the stress of very short seasons by maximizing relative development of reproductive tissues. (2) Short, high-harvest-index, oilseed plants selected in northern regions of Eurasia. (3) “Indica type” marijuana, an ancient semi-dwarf cultigen tracing to the Afghanistan-Pakistan area. (4) Semi-dwarf strains of marijuana bred illegally in recent decades to avoid detection when grown clandestinely indoors for the black market. Although the high THC content in marijuana strains limits their usage as germplasm for low-THC cultivars, modern breeding techniques can control this variable. The current elimination of all marijuana germplasm from breeding of hemp cultivars is short-sighted because marijuana biotypes possess a particularly wide range of genes. There is an urgent need to develop public gene bank collections of Cannabis.

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Photo by William P. Cunningham University of Minnesota and Mary Ann Cunningham Vassar College. Copyright © The McGraw-Hill Companies, Inc. Reproduced with permission

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Prepared by B. Brookes

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Prepared by B. Brookes

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Source: Vilmorin-Andrieux (1885)

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Photo by Bob Nichols, USDA (CC BY 2.0)

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Prepared by E. Small and T. Antle

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Credit: Nicolle Rager Fuller, National Science Foundation

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(Drawings by B. Brookes, photos by E. Small)

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Photo by E. Small

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Prepared by B. Brookes

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Photo courtesy of N.P. Schultes

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Photo by Transmitdistort (CC BY 3.0)

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US Government photo

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Photo courtesy of Professor Bócsa

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Prepared by B. Brookes

References

  1. Ainsworth C (2000) Boys and girls come out to play: the molecular biology of dioecious plants. Ann Bot 86:211–221

    Article  Google Scholar 

  2. Alonso-Blanco C, Blankestijn-De Vries H, Hanhart CJ, Koornneef M (1999) Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana. PNAS 96:4710–4717

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  3. Andre CM, Hausman J-F, Guerriero G (2016) Cannabis sativa: the plant of the thousand and one molecules. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00019

    PubMed  PubMed Central  Google Scholar 

  4. Anonymous (1859) Some remarks on monoecious and dioecious plants. Phytologist 3:257–259

    Google Scholar 

  5. Bócsa I (1998) Genetic improvement: conventional approaches. In: Ranalli P (ed) Advances in hemp research. Food Products Press (of Haworth Press), London, pp 153–184

    Google Scholar 

  6. Bossoreille De, de Ribou S, Douam F, Hamant O, Frohlich MW, Negrutiu I (2013) Plant science and agricultural productivity: why are we hitting the yield ceiling? Plant Sci 210:159–176

    Article  CAS  Google Scholar 

  7. Brickell CD, Alexander C, Cubey JJ, David JC, Hoffman MHA, Leslie AC, Malécot V et al (2016) International code of nomenclature for cultivated plants, 9th edn. International Society for Horticultural Science, Leuven

    Google Scholar 

  8. Callaway JC, Laakkonen TT (1996) Cultivation of Cannabis oil seed varieties in Finland. J Int Hemp Assoc 3(1):32–34

    Google Scholar 

  9. Carter PR, Hicks, DR, Oplinger, ES, Doll, JD, Bundy LG, Schuler, RT, Holmes BJ (1989) Grain sorghum (milo). Alternative field crops manual. Universities of Wisconsin and Minnesota. https://hort.purdue.edu/newcrop/afcm/sorghum.html

  10. Carus M (2016) Position paper of the European Industrial Hemp Association (EIHA) on: reasonable regulation of cannabidiol (CBD) in food, cosmetics, as herbal natural medicine and as medicinal product. European Industrial Hemp Asociation. http://eiha.org/media/2016/10/16-10-26-EIHA-CBD-position-paper.pdf

  11. Cherney JH, Small E (2016) Industrial hemp in North America: production, politics and potential. Agronomy 6(4), 58; https://doi.org/10.3390/agronomy6040058 http://www.mdpi.com/2073-4395/6/4/58/html

  12. Clarke RC (1981) Marijuana botany: an advanced study: the propagation and breeding of distinctive cannabis. And/Or Press, Berkeley

    Google Scholar 

  13. Clarke RC (1998) Hashish!. Red Eye Press, Los Angeles

    Google Scholar 

  14. Clarke RC, Merlin MD (2013) Cannabis: evolution and ethnobotany. University of California Press, Los Angeles

    Google Scholar 

  15. Clarke RC, Merlin MD (2016) Cannabis domestication, breeding history, present-day genetic diversity, and future prospects. Crit Rev Plant Sci 35:293–327

    Article  Google Scholar 

  16. Clarke RC, Watson DP (2006) Cannabis and natural Cannabis medicines. In: ElSohly MA (ed) Marijuana and the cannabinoids. Humana Press, Totowa, pp 1–17

    Google Scholar 

  17. Dairymple DG (1980) Development and spread of semi-dwarf varieties of wheat and rice in the United States. United States Department of Agriculture, Washington

    Google Scholar 

  18. Darby P (2005) The history of hop breeding and development. Brew Hist 121:94–112

    Google Scholar 

  19. De Meijer E (1994) Diversity in Cannabis. Wageningen Agricultural University, Wageningen. (Published doctoral thesis)

  20. De Meijer EPM (1995) Fibre hemp cultivars: a survey of origin, ancestry, availability and brief agronomic characteristics. J Int Hemp Assoc 2(2):66–73

    Google Scholar 

  21. De Meijer EPM, Hammond KM (2005) The inheritance of chemical phenotype in Cannabis sativa L. (II): canabigerol predominant plants. Euphytica 145:189–198

    Article  CAS  Google Scholar 

  22. De Meijer EPM, Bagatta M, Carboni A, Crucitti P, Moliterni VMC, Ranalli P, Mandolino G (2003) The inheritance of chemical phenotype in Cannabis sativa L. Genetics 163:335–346

    PubMed  PubMed Central  Google Scholar 

  23. De Meijer EPM, Hammond KM, Sutton A (2009) The inheritance of chemical phenotype in Cannabis sativa L. (IV): cannabinoid-free plants. Euphytica 168:95–112

    CAS  Article  Google Scholar 

  24. Dewey LH (1914) Hemp. In: US Department of Agriculture (corporate ed) Yearbook of the United States Department of Agriculture 1913. US Department of Agriculture, Washington, D.C. pp 283–347

  25. Dickmann DI, Gold MA, Flore JA (1994) The ideotype concept and the genetic improvement of tree crops. Plant Breed Rev 12:163–193

    Google Scholar 

  26. Divashuk MG, Alexandrov OS, Razumova OV, Kirov IV, Karlov GI (2014) Molecular cytogenetic characterization of the dioecious Cannabis sativa with an XY chromosome sex determination system. PLoS One 9(1):e85118. https://doi.org/10.1371/journal.pone.0085118

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  27. Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488

    CAS  PubMed  Article  Google Scholar 

  28. Donald CM (1968) The breeding of crop ideotypes. Euphytica 17:385–403

    Article  Google Scholar 

  29. Duc G, Agrama H, Bao S, Berger J, Bourion V, De Ron AM, Gowda CLL et al (2015) Breeeding annual grain legumes for sustainable agriculture: new methods to approach complex traits and target new cultivar ideotypes. Crit Rev Plant Sci 34:381–411

    Article  Google Scholar 

  30. ElSohly MA, Gul W (2014) Constituents of Cannabis sativa. In: Pertwee RG (ed) Handbook of cannabis. Oxford University Press, Oxford, pp 3–22

    Google Scholar 

  31. Faux A-M, Berhin A, Dauguet N, Bertin P (2014) Sex chromosomes and quantitative sex expression in monoecious hemp (Cannabis sativa L.). Euphytica 196:183–197

    Article  Google Scholar 

  32. Forster BP, Shub QY (2011) Plant mutagenesis in crop improvement: Basic terms and applications. In: Shu QY, Forster BP, Nakagawa H (eds) Plant mutation breeding and biotechnology. Food and Agriculture Organization, Rome, pp 9–20

    Google Scholar 

  33. Gardner F (2015/2016) Impeded by raids and bans, California producers strive to keep up with demand for CBD medicinals. O’Shaughnessy’s Winter:46, 68

  34. Glas JJ, Schimmel BCJ, Alba JM, Escobar-Bravo R, Schuurink RC, Kant MR (2012) Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int J Mol Sci 13:17077–17103

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. Grotenhermen F, Müller-Vahl K (2016) Medicinal uses of marijuana and cannabinoids. Crit Rev Plant Sci 35:378–405

    Article  Google Scholar 

  36. Hadley HH, Freeman JE, Javier EQ (1965) Effects of height mutations on grain yield in sorghum. Crop Sci 5:11–14

    Article  Google Scholar 

  37. Harper JL, Lovell PH, Moore KG (1970) The shapes and sizes of seeds. Ann Rev Ecol Syst 1:327–356

    Article  Google Scholar 

  38. Hedden P (2003a) Constructing dwarf rice. Nat Biotech 21:873–874

    CAS  Article  Google Scholar 

  39. Hedden P (2003b) The genes of the green revolution. Trends Genet 19:5–9

    CAS  PubMed  Article  Google Scholar 

  40. Henning J, Hill S, Darby P, Hendrix D (2017) QTL examination of a bi-parental mapping population segregating for ‘‘short-stature’’ in hop (Humulus lupulus L.). Euphytica 213:77. https://doi.org/10.1007/s10681-017-1848-x

    Article  CAS  Google Scholar 

  41. Hillig KW (2004) A multivariate analysis of allozyme variation in 93 Cannabis accessions from the VIR germplasm collection. J Indust Hemp 9(2):5–22

    CAS  Article  Google Scholar 

  42. Huyghe C (1998) Genetics and genetic modifications of plant architecture in grain legumes: a review. Agronomie 18:383–411

    Article  Google Scholar 

  43. Iffland K, Grotenhermen F (2017) An update on safety and side effects of cannabidiol: a review of clinical data and relevant animal studies. Cannabis Cannabinoid Res 2:1. https://doi.org/10.1089/can.2016.0034

    Article  Google Scholar 

  44. Inc Merriam-Webster (2012) Merriam-Webster’s Collegiate Dictionary, Eleventh edn. Merriam Webster Inc, Springfield

    Google Scholar 

  45. Jaradat AA (2007) Predictive grain yield models based on canopy structure and structural plasticity. Commun Biom Crop Sci 2:74–89

    Google Scholar 

  46. Kesavan M, Song JT, Seo HS (2013) Seed size: a priority trait in cereal crops. Physiol Plant 147:113–120

    CAS  PubMed  Article  Google Scholar 

  47. Klocko A, Stanton B, van Oosten C, Strauss SH (2013) Green revolution plantations: could short trees be a big thing? ISB News Report. http://www.isb.vt.edu/news/2013/May/GreenRevolutionPlantations.pdf

  48. Kupzow AJ (1975) Vavilov’s Law of Homologous Series at the fiftieth anniversary of its formulation. Econ Bot 29:372–379

    Article  Google Scholar 

  49. Lata H, Chandra S, Khan IA, Elsohly MA (2009) Propagation through alginate encapsulation of axillary buds of Cannabis sativa L.—an important medicinal plant. Physiol Mol Biol Plants 15:79–86

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. Lata H, Chandra S, Khan IA, Elsohly MA (2010) High frequency plant regeneration from leaf derived callus of high Δ9-tetrahydrocannabinol yielding Cannabis sativa L. Planta Med 76:1629–1633

    CAS  PubMed  Article  Google Scholar 

  51. Lata H, Chandra S, Techen N, Khan IA, ElSohly MA (2011) Molecular analysis of genetic fidelity in Cannabis sativa L. plants grown from synthetic (encapsulated) seeds following in vitro storage. Biotech Lett 33:2503–2508

    CAS  Article  Google Scholar 

  52. Lata H, Chandra S, Mehmedic Z, Khan IA, ElSohly MA (2012) In vitro germplasm conservation of high Δ9-tetrahydrocannabinol yielding elite clones of Cannabis sativa L. under slow growth conditions. Acta Physiol Plant 34:743–750

    CAS  Article  Google Scholar 

  53. Lee MA (2013) Medical marijuana, inc. Pitching CBD products. O’Shaughnessy’s Winter/Spring:23–24

  54. Mandolino G (2004) Again on the nature of inheritance of chemotype. Letter to the editor. J Indust Hemp 9(1):5–7

    Article  Google Scholar 

  55. Mandolino G, Ranalli P (2002) The applications of molecular markers in genetics and breeding of hemp. J Indust Hemp 7(1):7–23

    CAS  Article  Google Scholar 

  56. Mandolino G, Bagatta M, Carboni A, Ranalli P, de Meijer EPM (2003) Qualitative and quantitative aspects of the inheritance of chemical phenotype in Cannabis. J Indust Hemp 8(2):52–72

    Article  Google Scholar 

  57. Mao H, Sun S, Yao J, Wang C, Yu S, Xu C, Li X et al (2010) Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. PNAS 107:19579–19584

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. Mathan J, Bhattacharya J, Ranjan A (2016) Enhancing crop yield by optimizing plant developmental features. Development 143:3283–3294

    CAS  PubMed  Article  Google Scholar 

  59. McPartland JM, Guy GW (2004) The evolution of Cannabis and coevolution with the cannabinoid receptor—a hypothesis. In: Guy GW, Whittle BA, Robson PJ (eds) The medicinal uses of Cannabis and cannabinoids. Pharmaceutical Press, London, pp 71–101

    Google Scholar 

  60. McPartland JM, Guy GW (2017) Models of Cannabis taxonomy, cultural bias, and conflicts between scientific and vernacular names. Bot Rev. https://doi.org/10.1007/s12229-017-9187-0

    Google Scholar 

  61. McPartland JM, Clarke RC, Watson DP (2000) Hemp diseases and pests: management and biological control. CABI, Wallingford

    Book  Google Scholar 

  62. Milach SCK, Federizzi LC (2001) Dwarfing genes in plant improvement. Adv Agron 73:35–63

    CAS  Article  Google Scholar 

  63. Mölleken H, Husmann H (1997) Cannabinoids in seed extracts of Cannabis sativa cultivars. J Int Hemp Assoc 4(2):76–79

    Google Scholar 

  64. Mölleken H, Theimer RR (1997) Survey of minor fatty acids in Cannabis sativa L. fruits of various origins. J Int Hemp Assoc 4(1):13–17

    Google Scholar 

  65. Munro DB, Small E (1997) Vegetables of Canada. NRC Press, Ottawa

    Google Scholar 

  66. Nair P, Rao SK, Koutu GK (2013) Ideotype breeding in rice. JNKVV Res J 47:1–18

    Google Scholar 

  67. Neve RA (1991) Hops. Chapman and Hall, New York

    Book  Google Scholar 

  68. Niklas K (1994) Plant allometry: the scaling of form and process. University of Chicago Press, Chicago

    Google Scholar 

  69. O’Shaughnessy (O’Shaughnessy’s News Service) (2013) Project CBD update: the tango of supply and demand. O’Shaughnessy’s Winter/Spring:22–23

  70. Onofri C, de Meijer EPM, Mandolino G (2015) Sequence heterogeneity of cannabidiolic- and tetrahydrocannabinolic acid-synthase in Cannabis sativa L. and its relationship with chemical phenotype. Phytochemistry 116:57–68

    CAS  PubMed  Article  Google Scholar 

  71. Ordonio RL, Ito Y, Hatakeyama A, Ohmae-Shinohara K, Kasuga S, Tokunaga T, Mizuno H et al (2014) Gibberellin deficiency pleiotropically induces culm bending in sorghum: an insight into sorghum semi-dwarf breeding. Sci Rep 4:5287. https://doi.org/10.1038/srep05287

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  72. Pacifico D, Miselli F, Micheler M, Carboni A, Ranalli P, Mandolino G (2006) Genetics and marker-assisted selection of the chemotype in Cannabis sativa L. Mol Breed 17:257–268

    CAS  Article  Google Scholar 

  73. Patzak J, Dobrev PI, Motyka V (2013) Endogenous phytohormone levels in dwarf and normal hop (Humulus lupulus L.) plants. Acta Hort 1010:141–148

    Article  Google Scholar 

  74. Petri G, Oroszlán P, Fridvalszky L (1988) Histochemical detection of hemp trichomes and their correlation with the THC content. Acta Biol Hung 39:59–73

    CAS  PubMed  Google Scholar 

  75. Piluzza G, Delogu G, Cabras A, Marceddu S, Bullitta S (2013) Differentiation between fiber and drug types of hemp (Cannabis sativa L.) from a collection of wild and domesticated accessions. Genet Resour Crop Evol 60:2331–2342

    Article  Google Scholar 

  76. Pingali P (2012) Green revolution: impacts, limits and the path ahead. PNAS 109:12302–12308

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. Piperno DR, Ranere AJ, Holst I, Dickau R, Iriarte J (2009) Starch grain and phytolith evidence for early ninth millennium B.P. maize from the Central Balsas River Valley. Mexico PNAS 106:5019–5024

    CAS  PubMed  Article  Google Scholar 

  78. Potter D (2009) The propagation, characterisation and optimisation of Cannabis sativa L. as a phytopharmaceutical. King’s College, London. (Ph.D. thesis) http://www.gwpharm.com/publications-1.aspx

  79. Ranere AJ, Piperno DR, Holst I, Dickau R, Iriarte J (2009) The cultural and chronological context of early Holocene maize and squash domestication in the Central Balsas River Valley, Mexico. PNAS 106:5014–5018

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  80. Rasmusson DC (1987) An evaluation of ideotype breeding. Crop Sci 27:1140–1146

    Article  Google Scholar 

  81. Reekie EG, Bazzaz FA (2005) Reproductive allocation in plants. Elsevier, New York

    Google Scholar 

  82. Sakamoto T, Matsuoka M (2004) Generating high-yielding varieties by genetic manipulation of plant architecture. Curr Opin Biotechnol 15:144–147

    CAS  PubMed  Article  Google Scholar 

  83. Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M et al (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 134:1642–1653

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  84. Sangoi L, Salvador RJ (1998) Influence of plant height and of leaf number on maize production at high plant densities. Pesqui Agro Brasilaria 33:297–306

    Google Scholar 

  85. Sarlikioti V, de Visser PHB, Buck-Sorlin GH, Marcelis LFM (2011) How plant architecture affects light absorption and photosynthesis in tomato: towards an ideotype for plant architecture using a functional-structural plant model. Ann Bot 108:1065–1073

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  86. Sedgley RH (1991) An appraisal of the Donald ideotype after 21 years. Field Crops Res 26:93–112

    Article  Google Scholar 

  87. Small E (1972) Interfertility and chromosomal uniformity in Cannabis. Canad J Bot 50:1947–1949

    Article  Google Scholar 

  88. Small E (1975) Morphological variation of achenes of Cannabis. Canad J Bot 53:978–987

    Article  Google Scholar 

  89. Small E (2004) Narcotic plants as sources of medicinals, nutraceuticals, and functional foods. In: Hou F-F, Lin H-S, Chou M-H, Chang T-W (eds) Proceedings of the international symposium on the development of medicinal plants, 24–25 Aug. 2004, Hualien. Hualien District Agricultural Research and Extension Station, Hualien. pp 11–67

  90. Small E (2007) Cannabis as a source of medicinals, nutraceuticals, and functional foods. In: Acharya SN, Thomas JE (eds) Advances in medicinal plant research. Research Signpost/Transworld Research Network, Trivandrum, pp 1–39

    Google Scholar 

  91. Small E (2014) Hemp fiber and composites for the 21st century. In: Thakur VKT, Njuguna J (eds) Natural fibers and composites. Studium Press, Houston, pp 29–64

    Google Scholar 

  92. Small E (2015) Evolution and classification of Cannabis sativa (marijuana, hemp) in relation to human utilization. Bot Rev 81:189–294

    Article  Google Scholar 

  93. Small E (2016) Cannabis: a complete guide. Taylor & Francis/CRC Press, Boca Raton

    Book  Google Scholar 

  94. Small E (2017) Classification of Cannabis sativa in relation to agricultural, biotechnological, medical and recreational utilization. In: Chandra S, Lata H, ElSohly MA (eds) Cannabis sativa L.: botany and biotechnology. Springer-Verlag, Berlin, pp 1–62

    Google Scholar 

  95. Small E, Cronquist A (1976) A practical and natural taxonomy for Cannabis. Taxon 25:405–435

    Article  Google Scholar 

  96. Small E, Marcus D (2000) Hemp germplasm trials in Canada. In: Nova Institute (corporate ed) Proceedings third international symposium bioresource hemp. Nova Corporation Hürth. (Irregularly paginated)

  97. Small E, Marcus D (2002) Hemp—a new crop with new uses for North America. In: Janick J, Whipkey A (eds) Trends in new crops and new uses. ASHS Press, Alexandria, pp 284–326

    Google Scholar 

  98. Small E, Marcus D (2003) Tetrahydrocannabinol levels in hemp (Cannabis sativa) germplasm resources. Econ Bot 57:545–558

    CAS  Article  Google Scholar 

  99. Small E, Naraine SGU (2016) Size matters: evolution of large drug-secreting resin glands in elite pharmaceutical strains of Cannabis sativa (marijuana). Genet Resour Crop Evol 63:349–359

    Article  Google Scholar 

  100. Small E, Marcus D, McElroy A, Butler G (2007) Apparent increase in biomass and seed productivity in hemp (Cannabis sativa) resulting from branch proliferation caused by the European corn borer (Ostrinia nubilalis). J Indust Hemp 12(1):15–26

    Article  Google Scholar 

  101. Soroka VP (1978) Correlation between number of glandular hairs and content of cannabinoids in hemp. Referativnyi Zhurnal 6:528

    Google Scholar 

  102. Sytnik VP, Stelmah AF (1999) The character of inheritance of differences in cannabinoid content in hemp (Cannabis sativa L.). J Int Hemp Assoc 6(1):8–9

    Google Scholar 

  103. Szabó K, Sárosi S, Cserháti B, Ferenczy A (2010) Can glandular hair density be a breeding marker for Origanum vulgare subsp. hirtum with high essential oil content? Nat Prod Commun 5:1437–1440

    PubMed  Google Scholar 

  104. Tandon JP, Jain HK (2004) Plant ideotype: the concept and application. In: Jain HK, Kharkwal MC (eds) Plant breeding—Mendelian to molecular approaches. Narosa Publishing House, New Delhi, pp 585–600

    Google Scholar 

  105. Truong SK, McCormick RF, Rooney WL, Mullet JE (2015) Harnessing genetic variation in leaf angle to increase productivity of Sorghum bicolor. Genetics 201:1229–1238

    PubMed  PubMed Central  Article  Google Scholar 

  106. Turnbull CGN (ed) (2005) Plant architecture and its manipulation. Blackwell, Oxford

    Google Scholar 

  107. Turner JC, Hemphill JK, Mahlberg PG (1981a) Interrelationships of glandular trichomes and cannabinoid content. I: developing pistillate bracts of Cannabis sativa L. (Cannabaceae). Bull Narc 33:59–69

    CAS  PubMed  Google Scholar 

  108. Turner JC, Hemphill JK, Mahlberg PG (1981b) Interrelationships of glandular trichomes and cannabinoid content. II. Developing vegetative leaves of Cannabis sativa L. (Cannabaceae). Bull Narc 33:63–71

    CAS  PubMed  Google Scholar 

  109. Van Bakel H, Stout JM, Cote AG, Tallon CM, Sharpe AG, Hughes TR, Page JE (2011) The draft genome and transcriptome of Cannabis sativa. Genome Biology. https://doi.org/doi:10.1186/gb-2011-12-10-r102. http://genomebiology.com/content/pdf/gb-2011-12-10-r102.pdf

  110. Vilmorin-Andrieux MM (1885) The vegetable garden. John Murray, London

    Google Scholar 

  111. Wang Y, Li J (2008) Molecular basis of plant architecture. Ann Rev Plant Biol 59:253–279

    CAS  Article  Google Scholar 

  112. Watson DP, Clarke RC (1997) The genetic future of hemp. In: Nova Institute (corporate ed.) Proceedings of the bioresource hemp symposium, Frankfurt am Main, Germany, Feb. 27–March 2, 1997. Nova Institute, Hürth. pp. 122–127

  113. Weiblen GD, Wenger JP, Craft KJ, ElSohly MA, Mehmedic Z, Treiber EL, Marks MD (2015) Gene duplication and divergence affecting drug content in Cannabis sativa. New Phytol 208:1241–1250

    CAS  PubMed  Article  Google Scholar 

  114. Weiner J (2004) Allocation, plasticity and allometry in plants. Persp Plant Ecol Evol Syst 6:207–215

    Article  Google Scholar 

  115. Welling MT, Shapter T, Rose TJ, Liu L, Stanger R, King GJ (2016) A belated green revolution for Cannabis: virtual genetic resources to fast-track cultivar development. Front Plant Sci Jul 29;7:1113. https://doi.org/10.3389/fpls.2016.01113

  116. Yang X-C, Hwa C-M (2008) Genetic modification of plant architecture and variety improvement in rice. Heredity 101:396–404

    CAS  PubMed  Article  Google Scholar 

  117. Zhang Z, Liu Z, Hu Y, Li W, Fu Z, Ding D, Li H et al (2014) QTL analysis of kernel-related traits in maize using an immortalized F2 population. PLoS One 9:e89645

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  118. Zhao L, Tan L, Zhu Z, Xiao L, Xie D, Sun C (2015) PAY 1 improves plant architecture and enhances grain yield in rice. Plant J 83:528–536

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  119. Zohary D (2004) Unconscious selection and the evolution of domesticated plants. Econ Bot 58:5–10

    Article  Google Scholar 

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Small, E. Dwarf germplasm: the key to giant Cannabis hempseed and cannabinoid crops. Genet Resour Crop Evol 65, 1071–1107 (2018). https://doi.org/10.1007/s10722-017-0597-y

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Keywords

  • Cannabis sativa
  • Hemp
  • Hempseed
  • Marijuana
  • Dwarf
  • Semi-dwarf