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Plant and Soil

, Volume 425, Issue 1–2, pp 479–492 | Cite as

Rooting plasticity in wild and cultivated Andean Chenopodium species under soil water deficit

  • Ricardo Alvarez-Flores
  • Anh Nguyen-Thi-Truc
  • Santiago Peredo-Parada
  • Richard Joffre
  • Thierry Winkel
Regular Article

Abstract

Background and aims

Rooting plasticity is critical for plants exploiting patchy soil-water resources, but empirical evidence remains controversial due to complex root/soil interactions in natural and agricultural environments. We compared cultivated and wild Chenopodium populations from distinct agroecological background to assess their rooting plasticity when exposed to contrasting wet-dry soil profiles in a controlled environment.

Methods

Four treatments of increasing dryness were applied during 6 weeks in plants of Chenopodium hircinum, Chenopodium pallidicaule and two ecotypes (wet- and dry-habitat) of Chenopodium quinoa grown in rhizotrons. Root system architecture and growth were sequentially mapped. At the end of the experiment, plant and root morphological traits and dry biomass were measured.

Results

Contrary to the other two species, C. quinoa showed accelerated taproot growth in dry soil conditions. The dry-habitat C. quinoa ecotype showed consistently higher plant traits related to longer, coarser, and more numerous root segments which give it a faster taproot growth and sustained root branching at depth in dry soil.

Conclusions

High rooting plasticity confers the advantage of fast root elongation and deep soil exploration under soil water deficit. Variation in intrinsic root traits and plastic responses among Chenopodium populations controls their root foraging capacity facing patchy soil-water resources.

Keywords

Chenopodium quinoa C. hircinum C. pallidicaule Root architecture Rhizotron Natural and human selection 

Notes

Acknowledgements

This research was funded by a PhD grant of the “Capital Humano Avanzado” programme of CONICYT (Chile), by the ANR (Agence Nationale de la Recherche—The French National Research Agency, project ANR-06-PADD-011, EQUECO), and the collaborative program 2012-PCCI 12051 "Desarrollo de una perspectiva socioecológica para un rubro prometedor: la quínoa sostenible en Chile" between CONICYT (Chile) and IRD (France). We thank the staff of the Plateforme des Terrains d’Expériences and the Plateforme d’Analyses Chimiques en Écologie, technical facilities of the Labex CeMEB (ANR-10-LABX-0004-CeMEB) where the plants were grown and the root analyses done. We are most grateful to Felix Mamani Reynoso and Alejandro Bonifacio (Universidad Mayor de San Andrés, La Paz, Bolivia) for kindly providing the seeds of C. pallidicaule and C. hircinum, to Dr. Jairo A. Palta (CSIRO, Australia) for his detailed remarks and suggestions about this manuscript and to the anonymous reviewers for their constructive comments.

Supplementary material

11104_2018_3588_MOESM1_ESM.doc (66 kb)
ESM 1 (DOC 65 kb)

References

  1. Allard V, Martre P, Le Gouis J (2013) Genetic variability in biomass allocation to roots in wheat is mainly related to crop tillering dynamics and nitrogen status. Eur J Agron 46:68–76.  https://doi.org/10.1016/j.eja.2012.12.004 CrossRefGoogle Scholar
  2. Alvarez-Flores R, Winkel T, Degueldre D, Del Castillo C, Joffre R (2014a) Plant growth dynamics and root morphology of little-known species of Chenopodium from contrasted Andean habitats. Botany 92:101–108.  https://doi.org/10.1139/cjb-2013-0224 CrossRefGoogle Scholar
  3. Alvarez-Flores R, Winkel T, Nguyen-Thi-Truc A, Joffre R (2014b) Root foraging capacity depends on root system architecture and ontogeny in seedlings of three Andean Chenopodium species. Plant Soil 380:415–428.  https://doi.org/10.1007/s11104-014-2105-x CrossRefGoogle Scholar
  4. Bell LW, Williams AH, Ryan MH, Ewing MA (2007) Water relations and adaptations to increasing water deficit in three perennial legumes, Medicago sativa, Dorycnium hirsutum and Dorycnium rectum. Plant Soil 290:231–243.  https://doi.org/10.1007/s11104-006-9155-7 CrossRefGoogle Scholar
  5. Bosque Sanchez H, Lemeur R, Van Damme P, Jacobsen SE (2003) Ecophysiological analysis of drought and salinity stress of quinoa (Chenopodium quinoa Willd.) Food Rev Intl 19:111–119CrossRefGoogle Scholar
  6. Bouma TJ, Nielsen KL, Hal JV, Koutstaal B (2001) Root system topology and diameter distribution of species from habitats differing in inundation frequency. Funct Ecol 15:360–369.  https://doi.org/10.1046/j.1365-2435.2001.00523.x CrossRefGoogle Scholar
  7. Boyer JS, Silk WK, Watt M (2010) Path of water for root growth. Funct Plant Biol 37:1105–1116.  https://doi.org/10.1071/FP10108 CrossRefGoogle Scholar
  8. Bradshaw AD (2006) Unravelling phenotypic plasticity – why should we bother? New Phytol 170:644–648.  https://doi.org/10.1111/j.1469-8137.2006.01761.x CrossRefPubMedGoogle Scholar
  9. Cruz P, Winkel T, Ledru MP, Bernard C, Egan N, Swingedouw D, Joffre R (2017) Rain-fed agriculture thrived despite climate degradation in the pre-Hispanic arid Andes. Sci Adv 3:e1701740CrossRefPubMedPubMedCentralGoogle Scholar
  10. de Dorlodot S, Forster B, Pagès L, Price A, Tuberosa R, Draye X (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci 12:474–481CrossRefPubMedGoogle Scholar
  11. Fitter AH (1987) An architectural approach to the comparative ecology of plant root systems. New Phytol 106:61–77CrossRefGoogle Scholar
  12. Fitter AH, Stickland TR (1991) Architectural analysis of plant root systems 2. Influence of nutrient supply on architecture in contrasting plant species. New Phytol 118:383–389CrossRefGoogle Scholar
  13. Fitter AH, Stickland TR, Harvey ML, Wilson GW (1991) Architectural analysis of plant root systems. 1. Architectural correlates of exploitation efficiency. New Phytol 118:375–382CrossRefGoogle Scholar
  14. Glimskär A (2000) Estimates of root system topology of five plant species grown at steady-state nutrition. Plant Soil 227:249–256CrossRefGoogle Scholar
  15. Gregory PJ (2006) Plant roots : growth, activity, and interaction with soils. Blackwell Pub, OxfordCrossRefGoogle Scholar
  16. Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24.  https://doi.org/10.1111/j.1469-8137.2004.01015.x CrossRefGoogle Scholar
  17. Hodge A (2009) Root decisions. Plant Cell Environ 32:628–640CrossRefPubMedGoogle Scholar
  18. Ingram PA, Malamy JE (2010) Root system architecture. In: Kader J-C, Delseny M (eds) Advances in botanical research. Elsevier Academic Press, Burlington, Academic PressGoogle Scholar
  19. Ito K, Tanakamaru K, Morita S, Abe J, Inanaga S (2006) Lateral root development, including responses to soil drying, of maize (Zea mays) and wheat (Triticum aestivum) seminal roots. Physiol Plant 127:260–267.  https://doi.org/10.1111/j.1399-3054.2006.00657.x CrossRefGoogle Scholar
  20. Jensen CR, Jacobsen SE, Andersen MN, Núñez N, Andersen SD, Rasmussen L, Mogensen VO (2000) Leaf gas exchange and water relation characteristics of field quinoa (Chenopodium quinoa Willd.) during soil drying. Eur J Agron 13:11–25CrossRefGoogle Scholar
  21. King MJ, Bush LP (1985) Growth and water use of tall fescue as influenced by several soil drying cycles. Agron J 77.  https://doi.org/10.2134/agronj1985.00021962007700010001x
  22. Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press, San DiegoGoogle Scholar
  23. León MF, Squeo FA, Gutiérrez JR, Holmgren M (2011) Rapid root extension during water pulses enhances establishment of shrub seedlings in the Atacama Desert. J Veg Sci 22:120–129CrossRefGoogle Scholar
  24. Leva PE, Aguiar MR, Oesterheld M (2009) Underground ecology in a Patagonian steppe: root traits permit identification of graminoid species and classification into functional types. J Arid Environ 73:428–434.  https://doi.org/10.1016/j.jaridenv.2008.12.016 CrossRefGoogle Scholar
  25. Li R, Zeng Y, Xu J, Wang Q, Wu F, Cao M, Lan H, Liu Y, Lu Y (2015) Genetic variation for maize root architecture in response to drought stress at the seedling stage. Breed Sci 65:298–307.  https://doi.org/10.1270/jsbbs.65.298 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Liu L, Gan Y, Bueckert R, Van Rees K (2011) Rooting systems of oilseed and pulse crops I: temporal growth patterns across the plant developmental periods. Field Crop Res 122:256–263.  https://doi.org/10.1016/j.fcr.2011.04.002 CrossRefGoogle Scholar
  27. Lynch JP, Brown KM (2012) New roots for agriculture: exploiting the root phenome. Philos Trans R Soc B-Biol Sci 367:1598–1604.  https://doi.org/10.1098/rstb.2011.0243 CrossRefGoogle Scholar
  28. Materechera SA, Alston AM, Kirby JM, Dexter AR (1992) Influence of root diameter on the penetration of seminal roots into a compacted subsoil. Plant Soil 144:297–303.  https://doi.org/10.1007/bf00012888 CrossRefGoogle Scholar
  29. Moroke TS, Schwartz RC, Brown KW, Juo ASR (2005) Soil mater depletion and root distribution of three dryland crops. Soil Sci Soc Am J 69:197–205CrossRefGoogle Scholar
  30. National Research Council (1989) Lost crops of the Incas: little-known plants of the Andes with promise for worldwide cultivation. National Academy Press, Washington, D.C.Google Scholar
  31. Newman EI (1966) A method of estimating the total length of root in a sample. J Appl Ecol 3:139–145.  https://doi.org/10.2307/2401670 CrossRefGoogle Scholar
  32. Nibau C, Gibbs DJ, Coates JC (2008) Branching out in new directions: the control of root architecture by lateral root formation. New Phytol 179:595–614CrossRefPubMedGoogle Scholar
  33. Nicotra AN, Babicka NB, Westoby MW (2002) Seedling root anatomy and morphology: an examination of ecological differentiation with rainfall using phylogenetically independent contrasts. Oecologia 130:136–145.  https://doi.org/10.1007/s004420100788 CrossRefPubMedGoogle Scholar
  34. Ogawa A, Kawashima C, Yamauchi A (2005) Sugar accumulation along the seminal root axis, as affected by osmotic stress in maize: a possible physiological basis for plastic lateral root development. Plant Prod Sci 8:173–180CrossRefGoogle Scholar
  35. Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113.  https://doi.org/10.1146/annurev.arplant.58.032806.104006 CrossRefPubMedGoogle Scholar
  36. Padilla FM, Pugnaire FI (2007) Rooting depth and soil moisture control Mediterranean woody seedling survival during drought. Funct Ecol 21:489–495.  https://doi.org/10.1111/j.1365-2435.2007.01267.x CrossRefGoogle Scholar
  37. Pagès L, Vercambre G, Drouet J-L, Lecompte F, Collet C, Le Bot J (2004) Root Typ: a generic model to depict and analyse the root system architecture. Plant Soil 258:103–119.  https://doi.org/10.1023/b:plso.0000016540.47134.03 CrossRefGoogle Scholar
  38. Pagès L, Bécel C, Boukcim H, Moreau D, Nguyen C, Voisin A-S (2014) Calibration and evaluation of ArchiSimple, a simple model of root system architecture. Ecol Model 290:76–84.  https://doi.org/10.1016/j.ecolmodel.2013.11.014 CrossRefGoogle Scholar
  39. Palta J, Watt M (2009) Chapter 13 - Vigorous crop root systems: form and function for improving the capture of water and nutrients. In: Crop Physiology. Academic Press, San DiegoGoogle Scholar
  40. Palta JA, Chen X, Milroy SP, Rebetzke GJ, Dreccer MF, Watt M (2011) Large root systems: are they useful in adapting wheat to dry environments? Funct Plant Biol 38:347–354CrossRefGoogle Scholar
  41. Paula S, Pausas JG (2011) Root traits explain different foraging strategies between resprouting life histories. Oecologia 165:321–331.  https://doi.org/10.1007/s00442-010-1806-y CrossRefPubMedGoogle Scholar
  42. Poorter H, Ryser P (2015) The limits to leaf and root plasticity: what is so special about specific root length? New Phytol 206:1188–1190.  https://doi.org/10.1111/nph.13438 CrossRefPubMedGoogle Scholar
  43. Pregitzer KS, Laskowski MJ, Burton AJ, Lessard VC, Zak DR (1998) Variation in sugar maple root respiration with root diameter and soil depth. Tree Physiol 18:665–670.  https://doi.org/10.1093/treephys/18.10.665 CrossRefPubMedGoogle Scholar
  44. Price AH, Steele KA, Moore BJ, Jones RGW (2002) Upland rice grown in soil-filled chambers and exposed to contrasting water-deficit regimes II. Mapping quantitative trait loci for root morphology and distribution. Field Crop Res 76:25–43CrossRefGoogle Scholar
  45. Raja V, Bishnoi KC (1990) Evapotranspiration, water use efficiency, moisture extraction pattern and plant water relations of rape (Brassica campestris) genotypes in relation to root development under varying irrigation schedules. Exp Agric 26:227–233CrossRefGoogle Scholar
  46. Reader RJ, Jalili A, Grime JP, Spencer RE, Matthews N (1993) A comparative study of plasticity in seedling rooting depth in drying soil. J Ecol 81:543–550CrossRefGoogle Scholar
  47. Rich SM, Wasson AP, Richards RA, Katore T, Prashar R, Chowdhary R, Saxena DC, Mamrutha HM, Zwart A, Misra SC, Sai Prasad SV, Chatrath R, Christopher J, Watt M (2016) Wheats developed for high yield on stored soil moisture have deep vigorous root systems. Funct Plant Biol 43:173–188.  https://doi.org/10.1071/FP15182 CrossRefGoogle Scholar
  48. Richards R, Watt M, Rebetzke G (2007) Physiological traits and cereal germplasm for sustainable agricultural systems. Euphytica 154:409–425.  https://doi.org/10.1007/s10681-006-9286-1 CrossRefGoogle Scholar
  49. Sandhu N, Raman KA, Torres RO, Audebert A, Dardou A, Kumar A, Henry A (2016) Rice root architectural plasticity traits and genetic regions for adaptability to variable cultivation and stress conditions. Plant Physiol 171(2562).  https://doi.org/10.1104/pp.16.00705
  50. Sapkota TB, Askegaard M, Lægdsmand M, Olesen JE (2012) Effects of catch crop type and root depth on nitrogen leaching and yield of spring barley. Field Crop Res 125:129–138.  https://doi.org/10.1016/j.fcr.2011.09.009 CrossRefGoogle Scholar
  51. Saxton KE, Rawls WJ (2006) Soil water characteristic estimates by texture and organic matter for hydrologic solutions. Soil Sci Soc Am J 70:1569–1578CrossRefGoogle Scholar
  52. Schmidhalter U, Evéquoz M, Camp K-H, Studer C (1998) Sequence of drought response of maize seedlings in drying soil. Physiol Plant 104:159–168CrossRefGoogle Scholar
  53. Schwinning S, Sala OE (2004) Hierarchy of responses to resource pulses in arid and semi-arid ecosystems. Oecologia 141:211–220.  https://doi.org/10.1007/s00442-004-1520-8 CrossRefPubMedGoogle Scholar
  54. Smith S, De Smet I (2012) Root system architecture: insights from Arabidopsis and cereal crops. Philosophical Philos Trans R Soc, B 367:1441–1452CrossRefGoogle Scholar
  55. Suralta RR, Kano-Nakata M, Niones JM, Inukai Y, Kameoka E, Tran TT, Menge D, Mitsuya S, Yamauchi A (2016) Root plasticity for maintenance of productivity under abiotic stressed soil environments in rice: progress and prospects. Field Crop Res.  https://doi.org/10.1016/j.fcr.2016.06.023
  56. Tapia ME (2000) Mountain agrobiodiversity in Peru. Mt Res Dev 20:220–225. https://doi.org/10.1659/0276-4741(2000)020[0220:MAIP]2.0.CO;2Google Scholar
  57. Taub DR, Goldberg D (1996) Root system topology of plants from habitats differing in soil resource availability. Funct Ecol 10:258–264CrossRefGoogle Scholar
  58. Troll C (1968) Geo-ecology of the mountainous regions of the tropical americas. In: Troll C (ed) Colloquium Geographicum. UNESCO-LARC-IGU, MexicoGoogle Scholar
  59. Zimmerer KS (1998) The ecogeography of Andean potatoes. Bioscience 48:445–454.  https://doi.org/10.2307/1313242 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.CEFE (Centre d’Écologie Fonctionnelle et Évolutive), CNRS (Centre National de la Recherche Scientifique), EPHE (École Pratique des Hautes Études), IRD (Institut de Recherche pour le Développement)Université de Montpellier, UPVM3 (Université Paul-Valéry Montpellier III)MontpellierFrance
  2. 2.Departamento de Gestión Agraria, Facultad TecnológicaUSACH (Universidad de Santiago de Chile)SantiagoChile

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