Advertisement

Plant Ecology pp 203-256 | Cite as

Adverse Soil Mineral Availability

  • Ernst-Detlef Schulze
  • Erwin Beck
  • Nina Buchmann
  • Stephan Clemens
  • Klaus Müller-Hohenstein
  • Michael Scherer-Lorenzen
Chapter

Abstract

This chapter covers our molecular understanding of how plants acquire growth-limiting mineral nutrients and cope with the presence of potentially toxic elements in the soil. Plants rarely experience an ample supply of all 14 essential elements, which have to be taken up from an exceedingly complex system, the soil. Strategies to meet this challenge include tightly controlled nutrient uptake and the plasticity of root architecture. Nutrient status and external availability are constantly monitored and translated into changes in uptake capacity and root morphology. Symbioses are of major importance for plant nutrient acquisition. Mycorrhizae and nitrogen fixation are described in separate sections with respect to the molecular processes involved in partner recognition and establishment, as well as nutrient exchange. The final sections of the chapter elaborate on the mechanisms allowing adapted plants to thrive even when normally toxic concentrations of mostly non-essential elements such as sodium and aluminium are present in the soil. Large areas around the globe are affected by either salinization or the availability of aluminium because of low soil pH. Resistance is often mediated by exclusion of the element or sequestration in vacuoles. Finally, the rare ability of some plant species to hyperaccumulate metals in spite of their toxicity is introduced as an example of plant adaptation to extremely stressful environments.

References

  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefPubMedCentralGoogle Scholar
  2. Antonovics J, Bradshaw AD, Turner RG (1971) Heavy metal tolerance in plants. Adv Environ Sci Technol 7:1–85Google Scholar
  3. Apse MP, Blumwald E (2002) Engineering salt tolerance in plants. Curr Opin Biotechnol 13:146–150PubMedCrossRefPubMedCentralGoogle Scholar
  4. Baker AJMBRR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126Google Scholar
  5. Bassil E, Coku A, Blumwald E (2012) Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development. J Exp Bot 63:5727–5740PubMedCrossRefPubMedCentralGoogle Scholar
  6. Becher M, Talke IN, Krall L, Krämer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268PubMedCrossRefPubMedCentralGoogle Scholar
  7. Brumbarova T, Bauer P, Ivanov R (2015) Molecular mechanisms governing Arabidopsis iron uptake. Trends Plant Sci 20:124–133PubMedCrossRefPubMedCentralGoogle Scholar
  8. Buchanan B, Gruissem W, Jones R (2015) Biochemistry and molecular biology of plants, 2nd edn. Wiley, SomersetGoogle Scholar
  9. Bulgarelli D, Schlaeppi K, Spaepen S et al (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838PubMedCrossRefPubMedCentralGoogle Scholar
  10. Chérel I, Lefoulon C, Boeglin M, Sentenac H (2014) Molecular mechanisms involved in plant adaptation to low K(+) availability. J Exp Bot 65:833–848PubMedCrossRefPubMedCentralGoogle Scholar
  11. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719PubMedCrossRefPubMedCentralGoogle Scholar
  12. Clemens S (2001) Molecular mechanisms of plant metal homeostasis and tolerance. Planta 212:475–486PubMedPubMedCentralCrossRefGoogle Scholar
  13. Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512PubMedCrossRefPubMedCentralGoogle Scholar
  14. Clemens S, Weber M (2016) The essential role of coumarin secretion for Fe acquisition from alkaline soil. Plant Signal Behav 11:e1114197CrossRefGoogle Scholar
  15. Curie C, Panaviene Z, Loulergue C et al (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349PubMedCrossRefPubMedCentralGoogle Scholar
  16. Deinlein U, Stephan AB, Horie T et al (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379PubMedPubMedCentralCrossRefGoogle Scholar
  17. Delhaize E, Ma JF, Ryan PR (2012) Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci 17:341–348PubMedCrossRefPubMedCentralGoogle Scholar
  18. Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.). II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dreyer I, Blatt MR (2009) What makes a gate? The ins and outs of Kv-like K+ channels in plants. Trends Plant Sci 14:383–390PubMedCrossRefPubMedCentralGoogle Scholar
  20. Epstein E, Rains DW, Elzam OE (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc Natl Acad Sci U S A 49:684–692PubMedPubMedCentralCrossRefGoogle Scholar
  21. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963PubMedCrossRefPubMedCentralGoogle Scholar
  22. Foy CD, Chaney RL, White MC (1978) Physiology of metal toxicity in plants. Annu Rev Plant Physiol Plant Mol Biol 29:511–566CrossRefGoogle Scholar
  23. Frausto da Silva JJR, Williams RJP (2001) The biological chemistry of the elements: the inorganic chemistry of life. Oxford University Press, OxfordGoogle Scholar
  24. Garcia K, Doidy J, Zimmermann SD et al (2016) Take a trip through the plant and fungal transportome of mycorrhiza. Trends Plant Sci 21:937–950PubMedCrossRefPubMedCentralGoogle Scholar
  25. Giehl RFH, Gruber BD, von Wirén N (2014) It’s time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65:769–778PubMedCrossRefPubMedCentralGoogle Scholar
  26. Halimaa P, Lin Y-F, Ahonen V et al (2014) Gene expression differences between Noccaea caerulescens ecotypes help identifying candidate genes for metal phytoremediation. Environ Sci Technol 48(6):3344–3353Google Scholar
  27. Hanikenne M, Kroymann J, Trampczynska A et al (2013) Hard selective sweep and ectopic gene conversion in a gene cluster affording environmental adaptation. PLoS Genet 9:e1003707PubMedPubMedCentralCrossRefGoogle Scholar
  28. Hanikenne M, Talke IN, Haydon MJ et al (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395PubMedCrossRefPubMedCentralGoogle Scholar
  29. Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629PubMedCrossRefPubMedCentralGoogle Scholar
  30. Hart H (1930) Nicolas Theodore de Saussure. Plant Physiol 5:424–429PubMedPubMedCentralCrossRefGoogle Scholar
  31. Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499Google Scholar
  32. Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052PubMedCrossRefPubMedCentralGoogle Scholar
  33. Ho C-H, Lin S-H, Hu H-C, Tsay Y-F (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194PubMedCrossRefPubMedCentralGoogle Scholar
  34. Horie T, Karahara I, Katsuhara M (2012) Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants. Rice 5:11Google Scholar
  35. Irving H, Williams R (1948) Order of stability of metal complexes. Nature 162:746–747CrossRefGoogle Scholar
  36. Klein T, Siegwolf RTW, Körner C (2016) Belowground carbon trade among tall trees in a temperate forest. Science 352:342–344PubMedCrossRefPubMedCentralGoogle Scholar
  37. Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–152PubMedCrossRefGoogle Scholar
  38. Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493PubMedCrossRefGoogle Scholar
  39. Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598PubMedCrossRefGoogle Scholar
  40. Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534PubMedCrossRefPubMedCentralGoogle Scholar
  41. Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review. J Plant Nutr Soil Sci 163:421–431Google Scholar
  42. Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New YorkCrossRefGoogle Scholar
  43. Lambers H, Martinoia E, Renton M (2015) Plant adaptations to severely phosphorus-impoverished soils. Curr Opin Plant Biol 25:23–31PubMedCrossRefPubMedCentralGoogle Scholar
  44. Li J-Y, Liu J, Dong D et al (2014) Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. PNAS 111:6503–6508CrossRefGoogle Scholar
  45. Lin Y-F, Aarts MGM (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206PubMedCrossRefPubMedCentralGoogle Scholar
  46. López-Arredondo DL, Leyva-González MA, González-Morales SI et al (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123PubMedCrossRefPubMedCentralGoogle Scholar
  47. Lüttge U, Kluge M, Bauer G (2005) Botanik, 5th edn. VCH, WeinheimGoogle Scholar
  48. Ma J, Ryan P, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278PubMedCrossRefPubMedCentralGoogle Scholar
  49. Ma JF, Tamai K, Yamaji N et al (2006) A silicon transporter in rice. Nature 440:688–691PubMedCrossRefPubMedCentralGoogle Scholar
  50. Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397PubMedCrossRefPubMedCentralGoogle Scholar
  51. Ma JF, Zheng SJ, Matsumoto H, Hiradate S (1997) Detoxifying aluminium with buckwheat. Nature 390:569–570CrossRefGoogle Scholar
  52. Magalhaes JV, Liu J, Guimaraes CT et al (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1161PubMedCrossRefPubMedCentralGoogle Scholar
  53. Maillet F, Poinsot V, Andre O et al (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63PubMedCrossRefPubMedCentralGoogle Scholar
  54. Marschner P (2012) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic Press, AmsterdamGoogle Scholar
  55. Miller AJ, Cramer MD (2005) Root nitrogen acquisition and assimilation. Plant Soil 274:1–36CrossRefGoogle Scholar
  56. Miller AJ, Shen Q, Xu G (2009) Freeways in the plant: transporters for N, P and S and their regulation. Curr Opin Plant Biol 12:284–290PubMedCrossRefPubMedCentralGoogle Scholar
  57. Miwa K, Takano J, Omori H et al (2007) Plants tolerant of high boron levels. Science 318:1417PubMedCrossRefPubMedCentralGoogle Scholar
  58. Møller IS, Gilliham M, Jha D et al (2009) Shoot Na+ exclusion and increased salinity tolerance engineered by cell type–specific alteration of Na+ transport in Arabidopsis. Plant Cell Online 21:2163–2178PubMedPubMedCentralCrossRefGoogle Scholar
  59. Moons A, Prinsen E, Bauw G, Van Montagu M (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 9:2243–2259PubMedPubMedCentralGoogle Scholar
  60. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250PubMedCrossRefPubMedCentralGoogle Scholar
  61. Munns R, James RA, Xu B et al (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol 30:360–364PubMedCrossRefPubMedCentralGoogle Scholar
  62. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefPubMedCentralGoogle Scholar
  63. Nable RO, Banuelos GS, Paull JG (1997) Boron toxicity. Plant Soil 193:181–198Google Scholar
  64. Neumann G, Martinoia E (2002) Cluster roots—an underground adaptation for survival in extreme environments. Trends Plant Sci 7:162–167PubMedCrossRefPubMedCentralGoogle Scholar
  65. Oh D-H, Leidi E, Zhang Q et al (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 151:210–222PubMedPubMedCentralCrossRefGoogle Scholar
  66. Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263PubMedCrossRefPubMedCentralGoogle Scholar
  67. Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113PubMedCrossRefPubMedCentralGoogle Scholar
  68. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775PubMedCrossRefPubMedCentralGoogle Scholar
  69. Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590Google Scholar
  70. Römheld V, Marschner H (1986) Mobilization of iron in the rhizosphere of different plant species. Adv Plant Nutrition 2:155–204Google Scholar
  71. Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668PubMedCrossRefPubMedCentralGoogle Scholar
  72. Sasaki T, Yamamoto Y, Ezaki B et al (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653PubMedCrossRefPubMedCentralGoogle Scholar
  73. Stracke S, Kistner C, Yoshida S et al (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962PubMedCrossRefPubMedCentralGoogle Scholar
  74. Sutton T, Baumann U, Hayes J et al (2007) Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318:1446–1449CrossRefGoogle Scholar
  75. Svennerstam H, Jämtgård S, Ahmad I et al (2011) Transporters in Arabidopsis roots mediating uptake of amino acids at naturally occurring concentrations. New Phytol 191:459–467PubMedCrossRefPubMedCentralGoogle Scholar
  76. Taiz L, Zeiger E (2006) Plant physiology, 4th edn. Sinauer Associates, SunderlandGoogle Scholar
  77. Takahashi M, Nakanishi H, Kawasaki S et al (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat Biotechnol 19:466–469PubMedCrossRefPubMedCentralGoogle Scholar
  78. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527Google Scholar
  79. Tsay Y, Chiu C, Tsai C et al (2007) Nitrate transporters and peptide transporters. FEBS Lett 581:2290–2300PubMedCrossRefPubMedCentralGoogle Scholar
  80. van der Ent A, Baker AJM, Reeves RD et al (2012) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334CrossRefGoogle Scholar
  81. van der Heijden MGA, Martin FM, Selosse M-A, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423PubMedCrossRefPubMedCentralGoogle Scholar
  82. Vert G, Grotz N, Dedaldechamp F et al (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1233–1243CrossRefGoogle Scholar
  83. Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14PubMedCrossRefPubMedCentralGoogle Scholar
  84. Ward JM, Mäser P, Schroeder JI (2009) Plant ion channels: gene families, physiology, and functional genomics analyses. Annu Rev Physiol 71:59–82PubMedPubMedCentralCrossRefGoogle Scholar
  85. Weber M, Deinlein U, Fischer S et al (2013) A mutation in the Arabidopsis thaliana cell wall biosynthesis gene pectin methylesterase 3 as well as its aberrant expression cause hypersensitivity specifically to Zn. Plant J 76:151–164Google Scholar
  86. Weber M, Harada E, Vess C et al (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281PubMedCrossRefPubMedCentralGoogle Scholar
  87. Weiler E, Nover L (2008) Allgemeine und molekulare Botanik. Thieme, StuttgartCrossRefGoogle Scholar
  88. Yamaguchi T, Hamamoto S, Uozumi N (2013) Sodium transport system in plant cells. Front Plant Sci 4:410Google Scholar
  89. Yuan F, Yang H, Xue Y et al (2014) OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514:367–371PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Ernst-Detlef Schulze
    • 1
  • Erwin Beck
    • 2
  • Nina Buchmann
    • 3
  • Stephan Clemens
    • 2
  • Klaus Müller-Hohenstein
    • 4
  • Michael Scherer-Lorenzen
    • 5
  1. 1.Max Planck Institute for BiogeochemistryJenaGermany
  2. 2.Department of Plant PhysiologyUniversity of BayreuthBayreuthGermany
  3. 3.Department of Environmental Systems ScienceETH ZurichZurichSwitzerland
  4. 4.Department of BiogeographyUniversity of BayreuthBayreuthGermany
  5. 5.Chair of Geobotany, Faculty of BiologyUniversity of FreiburgFreiburgGermany

Personalised recommendations