In Vitro Cellular & Developmental Biology - Plant

, Volume 37, Issue 6, pp 730–741 | Cite as

Root-specific metabolism: The biology and biochemistry of underground organs

  • Harsh Pal Bais
  • Victor M. Loyola-Vargas
  • Hector E. Flores
  • Jorge M. Vivanco
Invited Review

Summary

The roots of higher plants comprise a metabolically active and largely unexplored biological frontier. Some of their prime features include the ability to synthesize a remarkably diverse group of secondary metabolites, and to adjust their metabolic activities in response to different abiotic and biotic stresses. This adjustment includes the ability to exude a wide array of micro- and macromolecules into the rhizosphere and to phytoremediate toxic metals, with the potential to affect and alter the relationships between plants and both beneficial and deleterious soil-borne pathogens. In the past, research on root biology has been hampered by the underground nature of roots and the lack of suitable experimental systems to study root-root and root-microbe communications. However, recent progress in growing roots in isolation with other elements of the rhizosphere has greatly facilitated the study of root-specific metabolism and contributed to our understanding of this organ.

Key words

roots biology biochemistry metabolism communication exudation fluorescence 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aird, E. L. H.; Hamill, J. D.; Rhodes, M. J. C. Cytogenetic analysis of hairy root cultures from a number of plant species transformed by Agrobacterium rhizogenes. Plant Cell Tiss. Organ Cult. 15:47–57; 1988.CrossRefGoogle Scholar
  2. Allan, E. J.; Stuchbury, T.; Mordue (Luntz), A. J. Azadirachta indica A. Juss (Neem Tree): in vitro culture, micropropagation and the production of Azadiractine and other secondary metabolites. In: Bajaj, Y. P. S., ed. Biotechnology in agriculture and forestry, medicinal and aromatic plants XI, vol. 43. Berlin: Springer-Verlag; 1999:11–41.Google Scholar
  3. Asada, Y.; Li, W.; Yoshikawa, T. X. Isoprenylated flavonoids from hairy root cultures of Glycyrrhiza glabra. Phytochemistry 47:389–392; 1999.CrossRefGoogle Scholar
  4. Bais, H. P.; Sudha, G.; Ravishankar, G. A. Influence of polyamines on growth and coumarin production in hairy root cultures of Cichorium intybus L. cv. Lucknow local. J. Plant Growth Regul. 18:33–37; 1999.PubMedCrossRefGoogle Scholar
  5. Baker, J. T.; Borris, R. P.; Carté, B.; Cordell, G. A.; Soejarto, D. D.; Cragg, G. M.; Gupta, M. P.; Iwu, M.M.; Madulid, D.R.; Tyler, V.E. Natural product drug discovery and development: new perspectives on international collaboration. J. Nat. Prod. 58:1325–1357; 1995.PubMedCrossRefGoogle Scholar
  6. Baldwin, I. T. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc. Natl Acad. Sci. USA 95:8113–8118; 1998.PubMedCrossRefGoogle Scholar
  7. Barber, D. A.; Martin J. K. The release of organic substances by cereal roots into soil. New Phytol. 76:69–80; 1976.CrossRefGoogle Scholar
  8. Bensky, D.; Gamble, A. Chinese herbal medicine. Seattle: Eastland Press; 1986;273 pp.Google Scholar
  9. Boehm, R.; Sommer, S.; Li, S. M.; Heide, L. Genetic engineering on shikonin biosynthesis: expression of the bacterial ubi A gene in Lithospermum erythrorhizon. Plant Cell Physiol. 41:911–919; 2000.PubMedCrossRefGoogle Scholar
  10. Borisjuk, N. V.; Komarnytsky, S.; Timeva, S.; Hemleben, V.; Gleba, Y.; Raskin, I. Production of recombinant proteins in plant root exudates. Nature Biotechnol. 17:466–469; 1999.CrossRefGoogle Scholar
  11. Borris, R. P. Natural products research: perspectives from a major pharmaceutical company. J. Ethnopharmacol. 51:29–38; 1996.PubMedCrossRefGoogle Scholar
  12. Brigham, L. A.; Michaels, P. J.; Flores, H. E. Cell-specific production and antimicrobial activity of naphthoquinones in roots of Lithospermum erythrorhizon. Plant Physiol. 119:417–428; 1999.PubMedCrossRefGoogle Scholar
  13. Brigham, L. A.; Woo, H. H.; Hawes, M. C. Differential expression of proteins and m-RNAs from border cells and root tips of pea. Plant Physiol. 109:457–463; 1995.PubMedGoogle Scholar
  14. Briskin, D. P. Medicinal plants and phytomedicines. Linking plant biochemistry and physiology to human health. Plant Physiol. 124:507–514; 2000.PubMedCrossRefGoogle Scholar
  15. Buee, M.; Rossignol, M.; Jauneau, A.; Ranjeva, R.; Becard, G. The presymbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol. Plant Microbe Interact. 6:693–698; 2000.Google Scholar
  16. Callaway, R. M.; Aschehoug, E. T. Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 90:521–523; 2000.CrossRefGoogle Scholar
  17. Canto-Canche, B.; Loyola-Vargas, M. Chemicals from roots, hairy roots, and their application. Adv. Exp. Med. Biol. 464:235–275; 1999.PubMedGoogle Scholar
  18. Chilton, M. D.; Tepfer, D. A.; Petit, A.; David, C.; Casse-Delbart, F.; Tempé, J. Agrobacterium rhizogenes inserts T-DNA into the genomes of the host plant root cells. Nature 295:432–434; 1982.CrossRefGoogle Scholar
  19. Cho, M. H.; Paik, Y. S.; Hahn, T. R. Physical stability of shikonin derivatives from the roots of Lithospermum erythrorhizon cultivated in Korea. J. Agric. Food Chem. 47:4117–4120; 1999.PubMedCrossRefGoogle Scholar
  20. Christen, P. Centralus species: in vitro culture and the production of valepotriates and other secondary metabolites. In: Bajaj, Y. P. S., ed. Biotechnology in agriculture and forestry, medicinal and aromatic plants XI, vol. 43. Berlin: Springer-Verlag; 1999;42–56.Google Scholar
  21. Clark, A. M. Natural products as a resource for new drugs. Pharm. Res. 13:1133–1141; 1996.PubMedCrossRefGoogle Scholar
  22. Cordell, G. A. Changing strategies in natural products chemistry. Phytochemistry 40:1585–1612; 1995.CrossRefGoogle Scholar
  23. Couillerot, E.; Caron, C.; Trentesaux, C.; Chenieux, J. C.; Audran, J. C. Fagara zanthoxyloides Lam. (Rutaceae): in vitro culture and production of benzophenanthridine and furoquinoline alanine. In: Bajaj, Y. P. S., ed. Biotechnology in agriculture and forestry, medicinal and aromatic plants XI, vol. 43. Berlin: Springer-Verlag; 1999:136–156.Google Scholar
  24. Curtis, W. R. Encyclopedia of cell technology. In: Spier, R. E., ed. Hairy roots, bioreactor growth. New York: John Wiley & Sons; 2000:827–841.Google Scholar
  25. De Sauza, N. J.; Shah, V. In: Wagner, H., Hikino, H., Farnsworth, N. R., eds. Economic and medicinal plant research, vol. 2. New York: Academic Press; 1998:1–15.Google Scholar
  26. Flores, H. E.; Brigham, L. A.; Vivanco, J. M. The future of radicle biology? Connecting roots, people, and scientists. In: Flores, H. E., Lynch, J. P., Eissensstat, D., eds. Radicle biology: advances and perspectives on the function of plant roots. Current topics in plant physiology 18. Rockville, MD: American Society of Plant Physiologists; 1997:320–339.Google Scholar
  27. Flores, H. E.; Filner, P. Metabolic relationships of putrescine, GABA, and alkaloids in cell and root cultures of Solanaceae. In: Neumann, K. H., Barz, W., Reinhard, E., eds. Primary and secondary metabolism of plant cell cultures. New York: Springer-Verlag; 1985:174–185.Google Scholar
  28. Flores, H. E.; Vivanco, J. M.; Loyola-Vargas, V. M. Radicle biochemistry: the biology of root-specific metabolism. Trends Plant Sci. 4:220–226; 1999.PubMedCrossRefGoogle Scholar
  29. Fujita, Y.; Tabata, M. Secondary metabolites from plant cells: pharmaceutical applications and progress in commercial production. In: Green, C. E., Somers, D. A., Hackett, W. P., Biesboer, D. D., eds. Plant cell and tissue culture. New York: Alan R. Liss; 1987:169–185.Google Scholar
  30. Fukui, H.; Feroj Hasan, A. F. M.; Ueoka, T.; Kyo, M. Formation and secretion of a new brown benzoquinone by hairy root cultures of Lithospermum erythrorhizon. Phytochemistry 47:1037–1039; 1998.CrossRefGoogle Scholar
  31. Gaddipati, J. P.; Mani, H.; Shefali, R. K.; Mathad, V. T.; Bhaduri, A. P.; Maheshwari, R. K. Inhibition of growth and regulation of IGFs and VEGF in human prostate cancer cell lines by shikonin analogue 93/637. Anticancer Res. 20:2547–2552; 2000.PubMedGoogle Scholar
  32. Giri, A.; Banerjee, S.; Ahuja, P. S.; Giri, C. C. Production of hairy roots in Aconitum heterophyllum Wall. using Agrobacterium rhizogenes. In Vitro Cell Dev. Biol. Plant 33:280–284; 1997.Google Scholar
  33. Glaser, V. Billion-dollar market blossoms as botanical take root. Nature Biotechnol. 17:17–18; 1999.CrossRefGoogle Scholar
  34. Gleba, D.; Borisjuk, N. V.; Borisjuk, L. G.; Kneer, R.; Poulev, A.; Skarzhinskaya, M.; Dushenkov, S.; Logendra, S.; Gleba, Y. Y.; Raskin, I. Use of plant roots for phytoremediation and molecular farming. Proc. Natl Acad. Sci. USA 96:5973–5977; 1999.PubMedCrossRefGoogle Scholar
  35. Hamill, J. D.; Parr, A. J.; Rhodes, M. J. C.; Robins, R. J.; Walton, N. J. New routes to plant secondary products. Biotechnology 5:800–804; 1987.CrossRefGoogle Scholar
  36. Handa, T. Genetic transformation of Antirrhinum majus L and inheritance of altered phenotype induced by Ri T-DNA. Plant Sci. 81:199–206; 1992.CrossRefGoogle Scholar
  37. Haran, S.; Logendra, S.; Seskar, M.; Bratanova, M.; Raskin, I. Characterization of Arabidopsis acid phosphatase promoter and regulation of acid phosphatase expression. Plant Physiol. 124:615–626; 2000.PubMedCrossRefGoogle Scholar
  38. Harvey, A. Strategies for discovering drugs from previously unexplored natural products. Drug Discov. Today 5:294–300; 2000.PubMedCrossRefGoogle Scholar
  39. Hashimoto, T.; Yamada, Y. Alkaloid biogenesis: molecular aspects. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45:257–285; 1994.Google Scholar
  40. Hawes, M. C.; Brigham, L. A.; Wen, F.; Woo, H.; Zhu, Y. Root border cells— phenomenology of signal exchange. In: Flores, H. E., Lynch, J. P., Eissensstat, D., eds. Radicle biology: advances and perspectives on the function of plant roots. Current topics in plant physiology 18. Rockville, MD: American Society of Plant Physiologists; 1997:210–219.Google Scholar
  41. Hibi, N.; Higashiguchi, S.; Hashimoto, T.; Yamada, Y. Gene statement in tobacco low-nicotine mutants. Plant Cell 6:723–735; 1994.PubMedCrossRefGoogle Scholar
  42. Huang, B.; North, G.; Nobel, P. S. Soil sheaths, photosynthate distribution to roots and rhizosphere water relations for Opuntia ficus-indica. Int. J. Plant Sci. 154:425–431; 1993.CrossRefGoogle Scholar
  43. Imanishi, S.; Hashizume, K.; Nakakita, M.; Kojima, H.; Matsubayashi, Y.; Hashimoto, T.; Sakagami, Y.; Yamada, Y.; Nakamura, K. Differential induction by methyl jasmonate of genes encoding ornithine decarboxylase and other enzymes involved in nicotine biosynthesis in tobacco cell cultures. Plant Mol. Biol. 38:1101–1111; 1998.PubMedCrossRefGoogle Scholar
  44. Inoue, M.; Nishimura, H.; Li, H. H.; Mizutani, J. Allelochemicals from Polygonum sachalinense FR. SCHM. (Polygonaceae). J. Chem. Ecol. 18:1833–1840; 1992.Google Scholar
  45. Ionkova, I.; Kartnig, T.; Alfermann, W. Cycloartane saponin production in hairy root cultures of Astragalus mongholicus. Phytochemistry 45:1597–1600; 1997.CrossRefGoogle Scholar
  46. Itoh, A.; Ikuta, Y.; Baba, Y.; Tanahashi, T.; Nagakura, N. Ipecac alkaloids from Cephaelis acuminata. Phytochemistry 52:1169–1176; 1999.PubMedCrossRefGoogle Scholar
  47. Kamnev, A. A.; van der Lelie, D. Chemical and biological parameters as tools to evaluate and improve heavy metal phytoremediation. Biosci. Rep. 20:239–258; 2000.PubMedCrossRefGoogle Scholar
  48. Lahana, R. How many leads from HTS? Drug Discov. Today 4:447–448; 1999.PubMedCrossRefGoogle Scholar
  49. Lee, K. H. Novel antitumor agents from higher plants. Med. Res. Rev. 19:569–596; 2001.CrossRefGoogle Scholar
  50. Maldonado-Mendoza, I. E.; Harrison, H. Establishment of monoaxenic root organ cultures. In: Flores, H. E., Lynch, J. P., Eissensstat, D., eds. Radical biology: advances and perspectives on the function of plant roots. Current topics in plant physiology 18. Rockville, MD: American Society of Plant Physiologists: 1997:496–498.Google Scholar
  51. Mantle, D.; Lennard, T. W.; Pickering, A. T. Therapeutic applications of medicinal plants in the treatment of breast cancer: a review of their pharmacology, efficacy and tolerability. Adverse Drug React. Toxicol. Rev. 19:223–240; 2000.PubMedGoogle Scholar
  52. Maraganore, J. M.; Joseph, J.; Bailey, M. C. Purification and characterization of trichosanthin: homology to the rich A chain and implications as to the mechanism of abortifacient activity. J. Biol. Chem. 262:11628–11633; 1987.PubMedGoogle Scholar
  53. McGrath, M. S.; Hwang, K. M.; caldwell, S. E.; Gaston, I.; Luk, K.-C.; Wu, P.; Ng, V. L.; Crowe, S.; Daniels, J.; Marsh, J.; Deinhart, T.; Lekas, P. V.; Vennari, J. C.; Yeung, H.-W. An inhibitor of human immunodeficiency virus replication in acutely and chronically infected cells of lymphocyte and mononuclear phagocyte lineage. Proc. Natl. Acad. Sci. USA 86:2844–2848; 1989.PubMedCrossRefGoogle Scholar
  54. Medina-Bolivar, F. B.; Flores, H. E. Selection for hyoscyamine and cinnamoyl putrescine overproduction in cell and root cultures of Hyoscyamus muticus. Plant Physiol. 108:1553–1560; 1995.PubMedGoogle Scholar
  55. Nardi, S.; Concheri, G.; Pizzeghello, D.; Sturaro, A.; Rella, R.; Parvoli, G. Soil organic matter mobilization by root exudates. Chemosphere 5:653–658; 2000.CrossRefGoogle Scholar
  56. Nathan, P. Can the cognitive enhancing effects of Ginkgo biloba be explained by its pharmacology? Med. Hypothesis 55:491–493; 2000.CrossRefGoogle Scholar
  57. Nin, S.; Bennici, A.; Roselli, G.; Mariotti, D.; Schiff, S. Agrobacterium-mediated transformation of Artemisia absinthium L. (wormwood) and production of secondary metabolites. Plant Cell Rep. 16:725–730; 1997.CrossRefGoogle Scholar
  58. Paiva, N. L. An introduction to the biosynthesis of chemicals used in plant microbe communication. J. Plant Growth Regul. 19:131–143; 2000.PubMedGoogle Scholar
  59. Pilon-Smits, E.; Pilon, M. Breeding mercury-breathing plants for environmental cleanup. Trends Plant Sci. 5:235–236; 2000.PubMedCrossRefGoogle Scholar
  60. Pisha, E.; Pezzuto, J. M. Fruits and vegetables containing compounds that demonstrate pharmacological activity in humans. In: Wagner, H., Farnsworth, N. R., eds. Economic medicinal plant research, vol. 6. San Diego: Academic Press; 1994:188–233.Google Scholar
  61. Reuter, H. D.; Sendl, A. Allium sativum and Allium ursinum: chemistry, pharmacology and medicinal applications. In: Wagner, H., Farnsworth, N. R., eds. Economic medicinal plant research, vol. 6, San Diego: Academic Press; 1994:55–113.Google Scholar
  62. Riechers, D. E.; Timko, M. P. Structure and expression of the gene family encoding putrescine N-methyltransferase in Nicotiana tabacum: new clues to the evolutionary origin of cultivated tobacco. Plant Mol. Biol. 41:387–401; 1999.PubMedCrossRefGoogle Scholar
  63. Roshina, V. V.; Roshina, V. D. The excretory functions of higher plants. Berlin: Springer-Verlag; 1993.Google Scholar
  64. Santos, P. M.; Figueiredo, C.; Margarida Oliveira, M.; Barroso, J. G.; Pedro, L. G.; Deans, S. G.; Younus, A. K. M.; Scheffer, J. J. C. Essential oils from hairy root cultures and from fruits and roots of Pimpinella anisum. Phytochemistry 48:455–460; 1998.CrossRefGoogle Scholar
  65. Sasaki, K.; Udagawa, A.; Ishimaru, H.; Hayashi, T.; Alfermann, A. W.; Nakanishi, F.; Shimomura, K. High forskolin production in hairy roots of Coleus forskohlii. Plant Cell Rep. 17:457–459; 1998.CrossRefGoogle Scholar
  66. Savary, B. J.; Flores, H. E. Biosynthesis of defense-related proteins in transformed root cultures of Trichosanthes kirilowii Maxim. var japonicum (Kitam.). Plant Physiol. 106:1195–1204; 1994.PubMedCrossRefGoogle Scholar
  67. Schiefelbein, J. W. Constructing a plant cell. The genetic control of root hair development. Plant Physiol. 124:1525–1531; 2000.PubMedCrossRefGoogle Scholar
  68. Schultze, M.; Kondorosi, E.; Ratet, P.; Buiré, M. Cell and molecular biology of Rhizobium-plant interactions. Int. Rev. Cyt. 156:1–75; 1994.CrossRefGoogle Scholar
  69. Simpson, B. B.; Conner-Ogorzaly, M. Economic botany. Plants in our world. New York: McGraw-Hill; 1986.Google Scholar
  70. Sommer, S.; Kohle, A.; Yazaki, K.; Shimomura, K.; Bechthold, A.; Heide, L. Genetic engineering of shikonin biosynthesis hairy root cultures of Lithospermum erythrorhizon transformed with the bacterial ubiC gene. Plant Mol. Biol. 39:683–693; 1999.PubMedCrossRefGoogle Scholar
  71. Stintzi, A.; Browse, J. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc. Natl Acad. Sci. USA 97:10625–10630; 2000.PubMedCrossRefGoogle Scholar
  72. Stotz, H. U.; Pittendrigh, B. R.; Kroymann, J.; Weniger, K.; Fritsche, J.; Bauke, A.; Mitchell-Olds, T. Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol. 124:1007–1018; 2000.PubMedCrossRefGoogle Scholar
  73. Strickland, J. A.; Orr, G. L.; Walsh, T. A. Inhibition of Diabrotica larval growth by patatin, the lipid hydrolase from potato tubers. Plant Physiol. 109:667–674; 1995.PubMedGoogle Scholar
  74. Tanaka, N.; Matsumoto, T. Regenerants from Ajuga hairy roots with high productivity of 20-hydroxyecdysone. Plant Cell Rep. 13:87–90; 1993.CrossRefGoogle Scholar
  75. Tepfer, D. Transformation of several species of higher plants by Agrobacterium rhizogenes: sexual transmission of the transformed genotype and phenotype. Cell 37:959–967; 1984.PubMedCrossRefGoogle Scholar
  76. Trieu, A. T.; van Buuren, M. L.; Harrison, M. J. Gene expression in mycorrhizal roots of Medicago truncatula. In: Flores, H. E., Lynch, J. P., Eissensstat, D., eds. Radicle biology: advances and perspectives on the function of plant roots. Current topics in plant physiology 18. Rockville, MD: American Society of Plant Physiologists; 1997: 498–500.Google Scholar
  77. Vivanco, J. M.; Savary, B. J.; Flores, H. E. Characterization of two novel type I ribosome-inactivating proteins from the storage roots of the Andean crop Mirabilis expansa. Plant Physiol. 119:1447–1456; 1999.PubMedCrossRefGoogle Scholar
  78. Waller, G. R.; Novacki, E. Alkaloid biology and metabolism in plants. New York: Plenum Press; 1977:294.Google Scholar
  79. Wongsamuth, R.; Doran, P. M. Hairy root as an expression system for production of antibodies. In: Doran, P. M., ed. Hairy roots culture and applications. Netherlands: Harwood Academic Press; 1997:89–97.Google Scholar
  80. Yamamoto, H.; Yazaki, K.; Inoue, K. Simultaneous analysis of shikimate derived secondary metabolites in Lithospermum erythrorhizon cell suspension cultures by HPLC. J. Chromatogr. B. Biomed. Sci. Appl. 738:3–15; 2000.PubMedCrossRefGoogle Scholar
  81. Zhou, Y.; Hirotani, M.; Yoshikawa, Y.; Furuya, T. Flavonoids and phenylethanoids from hairy root cultures of Scutelaria baicalensis. Phytochemistry 44:83–87; 1997.CrossRefGoogle Scholar
  82. Zhu, Y. L.; Pilon-Smits, E. A.; Tarun, A. S.; Weber, S. V.; Jounin, L.; Terry, N. Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing gamma glutamylcsteine synthetase. Plant Physiol. 121:1169–1178; 1999.PubMedCrossRefGoogle Scholar

Copyright information

© Society for In Vitro Biology 2001

Authors and Affiliations

  • Harsh Pal Bais
    • 1
  • Victor M. Loyola-Vargas
    • 2
  • Hector E. Flores
    • 3
  • Jorge M. Vivanco
    • 1
  1. 1.Department of Horticulture and Landscape ArchitectureColorado State UniversityFort Collins
  2. 2.Unidad de Biología ExperimentalCentro de Investigación Científica de Yucatán, MéridaYucatánMéxico
  3. 3.Department of Plant Pathology and Biotechnology InstituteThe Pennsylvania State UniversityUniversity Park

Personalised recommendations