Skip to main content
Log in

The root of the problem of perennials domestication: is selection for yield changing key root system traits required for ecological sustainability?

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

During the process of domestication of herbaceous seed-producing perennial crops, selection for high yield induces a shift in the resource-use strategy from conservative to acquisitive. So far, studies on plant domestication has been focussed on the response of aerial productivity rather than in roots. Here we aimed to keep track of changes in root, in order to prevent the loss of root traits contributing to plant survival and longevity.

Methods

Using the perennial forb Physaria as a model, we compared the root system and its capacity for acquisition and storage of high yield and stable yield selected plants and their wild counterpart.

Results

High-yield accessions showed higher N acquisition rate and lower amount of reserves in roots than stable and wild accessions. Structural differences in root systems may be partially responsible for differences in acquisition rate and storage among accessions.

Conclusions

High-yield plants maintained high acquisition rates and an acquisitive set of traits, but showed a lower investment in storage that might affect longevity and yield stability. Ideally, the root system ideotype of perennial crops for marginal lands should combine the storage capacity of wild plants (i.e., hierarchical allocation of TNC and N to roots) with the high acquisition capacity of high-yield accessions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arbuckle JL, Wothke W (1999) AMOS 4.0 User’s Guide. Chicago, Small Waters Corporation, USA

  • Aziz MM, Palta JA, Siddique KH, Sadras VO (2017) Five decades of selection for yield reduced root length density and increased nitrogen uptake per unit root length in Australian wheat varieties. Plant Soil 413:181–192

    Article  CAS  Google Scholar 

  • Balachowski JA, Bristiel PM, Volaire FA (2016) Summer dormancy, drought survival and functional resource acquisition strategies in California perennial grasses. Ann Botany 118:357–368

    Article  Google Scholar 

  • Bloom AJ, Chapin FSIII, Mooney HA (1985) Resource limitation in plants: an economic analogy. Annu Rev Ecol Syst 16:363–392

    Article  Google Scholar 

  • Brahim K, Ray DT, Dierig DA (1998) Growth and yield characteristics of Lesquerella fendleri as a function of plant density. Ind Crop Prod 9:63–71

    Article  Google Scholar 

  • Burton AL, Brown KM, Lynch JP (2013) Phenotypic diversity of root anatomical and architectural traits in Zea species. Crop Sci 53:1042–1055

    Article  Google Scholar 

  • Cabrera A (1994) Regiones fitogeográficas Argentinas. Enciclopedia Argentina de Agricultura y Jardinería. Tomo II. Pp. 85. Fascículo 1. Acme S.A.C.I

  • Chapin FS III, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447

    Article  Google Scholar 

  • Coleman JS, McConnaughay KDM, Ackerly DD (1994) Interpreting phenotypic variation in plants. Trends Ecol Evol 9:187–191

    Article  CAS  PubMed  Google Scholar 

  • Comas LH, Eissenstat DM (2004) Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species. Funct Ecol 18:388–397

    Article  Google Scholar 

  • Comas L, Becker S, Cruz VMV, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442

    Article  PubMed  PubMed Central  Google Scholar 

  • Cox M, Qualset CO, Rains DW (1985) Genetic variation for nitrogen assimilation and translocation in wheat II: nitrogen assimilation in relation to grain yield and protein. Crop Sci 25:435–440

    Article  CAS  Google Scholar 

  • Cox TS, Van Tassel DL, Cox CM, DeHaan LR (2010) Progress in breeding perennial grains. Crop Pasture Sci 61:513–521

    Article  Google Scholar 

  • Craine JM, Froehle J, Tilman DG, Wedin DA, Chapin FS III (2001) The relationships among root and leaf traits of 76 grassland species and relative abundance along fertility and disturbance gradients. Oikos 93:274–285

    Article  Google Scholar 

  • Crews TE, Blesh J, Culman SW, Hayes RC, Jensen ES, Mack MC, Peoples MB, Schipanski ME (2016) Going where no grains have gone before: from early to mid-succession. Agric Ecosyst Environ 223:223–238

    Article  Google Scholar 

  • Dawson LA, Thornton B, Pratt SM, Paterson E (2004) Morphological and topological responses of roots to defoliation and nitrogen supply in Lolium perenne and Festuca ovina. New Phytol 161:811–818

    Article  PubMed  Google Scholar 

  • DeHaan JM, Van Tassel DL, Cox TS (2005) Perennial grain crops: a synthesis of ecology and plant breeding. Renew Agric Syst 20:5–14

    Article  Google Scholar 

  • Dierig DA, Thompson AE, Nakayama FS (1993) Lesquerella commercialization efforts in the United States. Ind Crop Prod 1:289–293

    Article  Google Scholar 

  • Eissenstat DM, Wells CE, Yanai RD, Withbeck JL (2000) Building roots in changing environment: implications for root longevity. New Phytol 147:33–42

    Article  CAS  Google Scholar 

  • Eriksen J (2009) Soil sulfur cycling in temperate agricultural systems. Adv Agron 102:55–89

    Article  CAS  Google Scholar 

  • Fitter AH, Stickland TR, Harvey ML, Wilson GW (1991) Architectural analysis of plant root systems I. architectural correlates of exploitation efficiency. New Phytol 118:375–382

    Article  Google Scholar 

  • Freschet GT, Swart EM, Cornelissen JH (2015) Integrated plant phenotypic responses to contrasting above-and below-ground resources: key roles of specific leaf area and root mass fraction. New Phytol 206:1247–1260

    Article  CAS  PubMed  Google Scholar 

  • García MB, Ehrlén J (2002) Reproductive effort and herbivory timing in a perennial herb: fitness components at the individual and population levels. Am J Bot 89:1295–1302

    Article  PubMed  Google Scholar 

  • Garnett T, Conn V, Kaiser BN (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ 32:1272–1283

    Article  CAS  PubMed  Google Scholar 

  • Glover JD, Reganold JP, Bell W, Borevitz J, Brummer EC, Buckler ES, Cox CM, Crews TE, Culman SW, DeHaan LR, Eriksson D, Gill BS, Holland J, Hul F, Hulke BS, Ibrahim MH, Jackson W, Jones SS, Murray SC, Paterson AH, Ploschuk E, Sacks EJ, Snapp S, Tao D, Van Tassel DJ, Wade LJ, Wyse DL, Xu Y (2010) Increased food and ecosystem security via perennial grains. Science 328:1638–1639

    Article  CAS  PubMed  Google Scholar 

  • González-Paleo L (2010) Cambios en atributos eco-fisiológicos asociados a la supervivencia, la perennidad y la estabilidad del rendimiento, resultantes del incremento del rendimiento por selección en especies anuales y perennes de Lesquerella (BRASSICACEA). PhD Thesis, Universidad de Buenos Aires, Buenos Aires

  • González-Paleo L, Ravetta DA (2011) Indirect changes associated with a selection program for increased seed-yield in wild species of Lesquerella (Brassicaceae): are we developing a phenotype opposite to the expected ideotype? Ind Crop Prod 34:1372–1380

    Article  Google Scholar 

  • González-Paleo L, Ravetta DA (2015) Carbon acquisition strategies uncoupled from predictions derived from species life-cycle. Flora 212:1–9

    Article  Google Scholar 

  • González-Paleo L, Vilela AE, Ravetta DA (2016) Back to perennials: does selection enhance tradeoffs between yield and longevity? Ind Crop Prod 91:272–278

    Article  Google Scholar 

  • Graham JH, Syvertsen JP (1985) Host determinants of mycorrhizal dependency of citrus rootstock seedlings. New Phytol 101:667–676

    Article  Google Scholar 

  • Greub LJ, Wedin WF (1971) Leaf area, dry-matter production, and carbohydrate reserve levels of Birdsfoot trefoil as influenced by cutting height. Crop Sci 11:734–738

    Article  Google Scholar 

  • Hernández EI, Vilagrosa A, Pausas JG, Bellot J (2010) Morphological traits and water use strategies in seedlings of Mediterranean coexisting species. Plant Ecol 207:233–244

    Article  Google Scholar 

  • Kaien R, Fumitaka S, Jun A, Shigenori M (2012) Biomass yield and nitrogen use efficiency of cellulosic energy crops for ethanol production. Biomass Bioenergy 37:330–334

    Article  CAS  Google Scholar 

  • Kell DB (2011) Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water sequestration. Ann Botany 108:407–418

    Article  CAS  Google Scholar 

  • Latzel V, Janeček Š, Doležal J, Klimešová J, Bossdorf O (2014) Adaptive transgenerational plasticity in the perennial Plantago lanceolata. Oikos 123:41–46

    Article  Google Scholar 

  • Loades KW, Bengough AG, Bransby MF, Hallett PD (2010) Planting density influence on fibrous root reinforcement of soils. Ecol Eng 36:276–284

    Article  Google Scholar 

  • Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Botany 112:347–357

    Article  CAS  Google Scholar 

  • Lynch JP, Brown KM (2008) Root strategies for phosphorus acquisition. In: The ecophysiology of plant-phosphorus interactions. Springer, Netherlands, pp 83–116

    Chapter  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518

    Article  PubMed  Google Scholar 

  • Milla R, Morente-López J, Alonso-Rodrigo JM, Martín-Robles N, Chapin FS III (2014) Shifts and disruptions in resource-use trait syndromes during the evolution of herbaceous crops. Proc R Soc B 281:20141429

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitchell RJ (1992) Testing evolutionary and ecological hypotheses using path analysis and structural equation modelling. Funct Ecol 6:123–129

    Article  Google Scholar 

  • Olmo M, Villar R, Salazar P, Alburquerque JA (2016) Changes in soil nutrient availability explain biochar’s impact on wheat root development. Plant Soil 399:333–343

    Article  CAS  Google Scholar 

  • Pastor-Pastor A, Vilela AE, González-Paleo L (2018) Tradeoffs between productivity and nitrogen conservation in wild and domesticated plants of the perennial crop Physaria (Brassicaceae). Ann Appl Biol 173:121–132

    Article  CAS  Google Scholar 

  • Paula S, Pausas JG (2011) Root traits explain different foraging strategies between resprouting life histories. Oecol 165:321–331

    Article  Google Scholar 

  • Pérez-Ramos IM, Volaire F, Fattet M, Blanchard A, Roumet C (2013) Tradeoffs between functional strategies for resource-use and drought-survival in Mediterranean rangeland species. Environ Exper Bot 87:126–136

    Article  Google Scholar 

  • Ploschuk EL, Windauer L, Ravetta DA (2001) Potential value of traits associated with perennial habit in the development of new oil-seed crops for arid lands. A comparison of Lesquerella fendleri and L. mendocina subjected to water stress. J Arid Environ 47:373–386

    Article  Google Scholar 

  • Ravetta DA, Soriano A (1998) Alternatives for the development of new industrial crops for Patagonia. Ecol Austral 8:297–307

    Google Scholar 

  • Reich PB, Tjoelker MG, Walters MB, Vanderklein DW, Buschena C (1998) Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Funct Ecol 12:327–338

    Article  Google Scholar 

  • Roumet C, Urcelay C, Díaz S (2006) Suites of root traits differ between annual and perennial species growing in the field. New Phytol 170:357–368

    Article  PubMed  Google Scholar 

  • Ryser P (1996) The importance of tissue density for growth and life span of leaves and roots: a comparison of five ecologically contrasting grasses. Funct Ecol 10:717–723

    Article  Google Scholar 

  • Ryser P (1998) Intra- and interspecific variation in root length, root turnover and the underlying parameters. In: Lambers H, Poorter H, Van Vuuren MMI (eds) Variation in plant growth. Backhuys Publishers. Leiden, pp 441–465

  • Ryser P (2006) The mysterious root length. Plant Soil 286:1–6

    Article  CAS  Google Scholar 

  • Scales FM, Harrison AP (1920) Boric acid modification of the Kjeldahl method for crop and soil analysis. Ind Eng Chem Res 12:350–352

    CAS  Google Scholar 

  • Smith D, Silva JP (1969) Use of carbohydrate and nitrogen root reserves in the regrowth of alfalfa from greenhouse experiments under light and dark conditions. Crop Sci 9:464–467

    Article  Google Scholar 

  • Thompson AE, Dierig DA (1994) Initial selection and breeding of Lesquerella fendleri, a new industrial oilseed. Ind Crop Prod 2:97–106

    Article  Google Scholar 

  • Tjoelker MG, Craine JM, Wedin D, Reich PB, Tilman D (2005) Linking leaf and root trait syndromes among 39 grassland and savannah species. New Phytol 167:493–508

    Article  CAS  PubMed  Google Scholar 

  • Trubat R, Cortina J, Vilagrosa A (2012) Root architecture and hydraulic conductance in nutrient deprived Pistacia lentiscus L. seedlings. Oecol 70:899–908

    Article  Google Scholar 

  • Vico G, Manzoni S, Nkurunziza L, Murphy K, Weih M (2016) Trade-offs between seed output and life span–a quantitative comparison of traits between annual and perennial congeneric species. New Phytol 209:104–114

    Article  CAS  PubMed  Google Scholar 

  • Vilela AE, González-Paleo L (2015) Changes in resource-use strategy and phenotypic plasticity associated with selection for yield in wild species native to arid environments. J Arid Environ 113:51–58

    Article  Google Scholar 

  • Wahl S, Ryser P (2000) Root tissue structure is linked to ecological strategies of grasses. New Phytol 148:459–471

    Article  PubMed  Google Scholar 

  • Weih M, Asplund L, Bergkvist G (2011) Assessment of nutrient use in annual and perennial crops: a functional concept for analyzing nitrogen use efficiency. Plant Soil 339:513–520

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • White TA, Snow VO (2012) A modelling analysis to identify plant traits for enhanced water-use efficiency of pasture. Crop Pasture Sci 63:63–76

    Article  Google Scholar 

  • White PJ, George TS, Gregory PJ, Bengough AG, Hallett PD, McKenzie BM (2013) Matching roots to their environment. Ann botany 112:207–222

    Article  CAS  Google Scholar 

  • Wissuwa M, Mazzola M, Picard C (2009) Novel approaches in plant breeding for rhizosphere-related traits. Plant Soil 321:409–430

    Article  CAS  Google Scholar 

  • Withington JM, Reich PB, Oleksyn J, Eissenstat DM (2006) Comparisons of structure and life span in roots and leaves among temperate trees. Ecol Monogr 76:381–397

    Article  Google Scholar 

  • Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182

    Article  CAS  PubMed  Google Scholar 

  • Yemm EW, Willis AJ (1954) Estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by Fondo Para la Investigación Científica y Tecnológica, PICT 2011 0598, and Consejo Nacional de Investigaciones Científicas y Técnicas, PIP 112 2011 0100780.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Pastor-Pastor.

Ethics declarations

Human and animal studies

This article does not contain any studies with human or animal subjects.

Conflict of interest

The authors declare that they do not have conflicts of interest.

Additional information

Responsible Editor: Anton Wasson.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pastor-Pastor, A., Vilela, A.E. & González-Paleo, L. The root of the problem of perennials domestication: is selection for yield changing key root system traits required for ecological sustainability?. Plant Soil 435, 161–174 (2019). https://doi.org/10.1007/s11104-018-3885-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3885-1

Keywords

Navigation