Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Evolutionary divergences in root system morphology, allocation, and nitrogen uptake in species from high- versus low-fertility soils

Alan W. Bowsher A C , Benjamin J. Miller B and Lisa A. Donovan A
+ Author Affiliations
- Author Affiliations

A 2502 Miller Plant Sciences, Department of Plant Biology, University of Georgia, Athens, GA 30602, USA.

B 400 Biosciences Building, Division of Biological Sciences, University of Georgia, Athens, GA 30602, USA.

C Corresponding author. Email: bowsher@uga.edu

Functional Plant Biology 43(2) 129-140 https://doi.org/10.1071/FP15162
Submitted: 13 June 2015  Accepted: 29 October 2015   Published: 9 December 2015

Abstract

Root morphology and nutrient uptake processes are essential for acquisition of mineral resources from soil. However, our understanding of how root form and function have diverged across environments is limited. In this study, we addressed hypotheses of adaptive differentiation using three pairs of Helianthus species chosen as phylogenetically-independent contrasts with respect to native soil nutrients. Under controlled environmental conditions, root morphology, allocation, and nitrogen (N) uptake (using a 15N tracer) were assessed for seedlings under both high and low N treatments. Species native to low nutrient soils (LNS) had lower total root length than those native to high nutrient soils (HNS), reflecting the slower growth rates of species from less fertile environments. Contrary to expectations, species did not consistently differ in specific root length, root tissue density, or root system plasticity, and species native to LNS had lower root : total mass ratio and higher 15N uptake rates than species native to HNS. Overall, these evolutionary divergences provide support for adaptive differentiation among species, with repeated evolution of slow-growing root systems suited for low resource availability in LNS. However, species native to LNS maintain a high capacity for N uptake, potentially as a means of maximising nutrient acquisition from transient pulses.

Additional keywords: adaptation, plant growth strategies, specific root length, stable isotopes, 15N.


References

Aerts R, Chapin FS (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30, 1–67.
The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns.Crossref | GoogleScholarGoogle Scholar |

Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta D, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141, 221–235.
Water pulses and biogeochemical cycles in arid and semiarid ecosystems.Crossref | GoogleScholarGoogle Scholar | 14986096PubMed |

Bloom AJ (1985) Wild and cultivated barleys show similar affinities for mineral nitrogen. Oecologia 65, 555–557.
Wild and cultivated barleys show similar affinities for mineral nitrogen.Crossref | GoogleScholarGoogle Scholar |

Boot RGA, Mensink M (1990) Size and morphology of root systems of perennial grasses from contrasting habitats as affected by nitrogen supply. Plant and Soil 129, 291–299.
Size and morphology of root systems of perennial grasses from contrasting habitats as affected by nitrogen supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXht1Srsr8%3D&md5=0e8b62e3c0bd636753bb0e8cb7bf3a5aCAS |

Campbell BD, Grime JP (1989) A comparative study of plant responsiveness to the duration of episodes of mineral nutrient enrichment. New Phytologist 112, 261–267.
A comparative study of plant responsiveness to the duration of episodes of mineral nutrient enrichment.Crossref | GoogleScholarGoogle Scholar |

Campbell BD, Grime JP, Mackey JML (1991) A trade-off between scale and precision in resource foraging. Oecologia 87, 532–538.
A trade-off between scale and precision in resource foraging.Crossref | GoogleScholarGoogle Scholar |

Chandler JM, Jan C-C, Beard BH (1986) Chromosomal differentiation among the annual Helianthus species. Systematic Botany 11, 354–371.
Chromosomal differentiation among the annual Helianthus species.Crossref | GoogleScholarGoogle Scholar |

Chapin FS (1980) The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11, 233–260.
The mineral nutrition of wild plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXivFagug%3D%3D&md5=f7671a6926cfca7687a22c4526c53bdaCAS |

Chapin FS (1988) Ecological aspects of plant mineral nutrition. Advances in Mineral Nutrition 3, 61–191.

Chen W, Zeng H, Eissenstat DM, Guo D (2013) Variation in first-order root traits across climatic gradients and evolutionary trends in geological time. Global Ecology and Biogeography 22, 846–856.
Variation in first-order root traits across climatic gradients and evolutionary trends in geological time.Crossref | GoogleScholarGoogle Scholar |

Christie EK, Moorby J (1975) Physiological responses of semiarid grasses. I. The influence of phosphorus supply on growth and phosphorus absorption. Australian Journal of Agricultural Research 26, 423–436.
Physiological responses of semiarid grasses. I. The influence of phosphorus supply on growth and phosphorus absorption.Crossref | GoogleScholarGoogle Scholar |

Comas LH, Eissenstat DM (2004) Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species. Functional Ecology 18, 388–397.
Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species.Crossref | GoogleScholarGoogle Scholar |

Comas LH, Bouma TJ, Eissenstat DM (2002) Linking root traits to potential growth rate in six temperate tree species. Oecologia 132, 34–43.
Linking root traits to potential growth rate in six temperate tree species.Crossref | GoogleScholarGoogle Scholar |

Comas LH, Mueller KE, Taylor LL, Midford PE, Callahan HS, Beerling DJ (2012) Evolutionary patterns and biogeochemical significance of angiosperm root traits. International Journal of Plant Sciences 173, 584–595.
Evolutionary patterns and biogeochemical significance of angiosperm root traits.Crossref | GoogleScholarGoogle Scholar |

Comas LH, Callahan HS, Midford PE (2014) Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies. Ecology and Evolution 4, 2979–2990.
Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies.Crossref | GoogleScholarGoogle Scholar | 25247056PubMed |

Craine JM, Dybzinski R (2013) Mechanisms of plant competition for nutrients, water, and light. Functional Ecology 27, 833–840.
Mechanisms of plant competition for nutrients, water, and light.Crossref | GoogleScholarGoogle Scholar |

Crick JC, Grime JP (1987) Morphological plasticity and mineral nutrient capture in two herbaceous species of contrasted ecology. New Phytologist 107, 403–414.
Morphological plasticity and mineral nutrient capture in two herbaceous species of contrasted ecology.Crossref | GoogleScholarGoogle Scholar |

Cunningham SA, Summerhayes B, Westoby M (1999) Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecological Monographs 69, 569–588.
Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients.Crossref | GoogleScholarGoogle Scholar |

Donovan LA, Mason CM, Bowsher AW, Goolsby EW, Ishibashi CDA (2014) Ecological and evolutionary lability of plant traits affecting carbon and nutrient cycling. Journal of Ecology 102, 302–314.
Ecological and evolutionary lability of plant traits affecting carbon and nutrient cycling.Crossref | GoogleScholarGoogle Scholar |

Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. Journal of Plant Nutrition 15, 763–782.
Costs and benefits of constructing roots of small diameter.Crossref | GoogleScholarGoogle Scholar |

Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Advances in Ecological Research 27, 1–60.
The ecology of root lifespan.Crossref | GoogleScholarGoogle Scholar |

Elberse WT, Berendse F (1993) A comparative study of the growth and morphology of eight grass species from habitats with different nutrient availabilities. Functional Ecology 7, 223–229.
A comparative study of the growth and morphology of eight grass species from habitats with different nutrient availabilities.Crossref | GoogleScholarGoogle Scholar |

Epstein E, Bloom AJ (2005) ‘Mineral nutrition of plants: principles and perspectives.’ (Sinauer Associates: Sunderland, MA, USA)

Fort F, Jouany C, Cruz P (2013) Root and leaf functional trait relation in Poaceae species: implication of differing resource-acquisition strategies. Journal of Plant Ecology 6, 211–219.
Root and leaf functional trait relation in Poaceae species: implication of differing resource-acquisition strategies.Crossref | GoogleScholarGoogle Scholar |

Fransen B, Blijjenberg J, de Kroon H (1999) Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches. Plant and Soil 211, 179–189.
Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntlKisL0%3D&md5=4148b336aad24fa4203cb0319d2d5182CAS |

Freschet GT, Swart EM, Cornelissen JHC (2015) Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction. New Phytologist 206, 1247–1260.
Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXotFCiu7g%3D&md5=de00e62fec530f80ebfbad8f77b1ba53CAS | 25783781PubMed |

Giehl RFH, von Wirén N (2014) Root nutrient foraging. Plant Physiology 166, 509–517.
Root nutrient foraging.Crossref | GoogleScholarGoogle Scholar |

Gioseffi E, de Neergaard A, Schjoerring JK (2012) Interactions between uptake of amino acids and inorganic nitrogen in wheat plants. Biogeosciences 9, 1509–1518.
Interactions between uptake of amino acids and inorganic nitrogen in wheat plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Gks7vK&md5=684e4e9973ddacac890d2e6a8f4ceb5bCAS |

Gotthard K, Nylin S (1995) Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos 74, 3–17.
Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history.Crossref | GoogleScholarGoogle Scholar |

Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111, 1169–1194.
Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory.Crossref | GoogleScholarGoogle Scholar |

Grime JP (1979) ‘Plant strategies and vegetation processes.’ (Wiley & Sons: Chichester, UK)

Grime JP (1994) The role of plasticity in exploiting environmental heterogeneity. In ‘Exploitation of environmental heterogeneity by plants: ecophysiological processes above- and belowground’. (Eds MM Caldwell, RW Pearcy) pp. 1–19. (Academic Press: San Diego, CA, USA)

Grime JP, Crick JC, Rincon JE (1986) The ecological significance of plasticity. In ‘Plasticity in plants’. (Eds DH Jennings, AJ Trewavas) pp. 5–19. (Company of Biologists: Cambridge, UK)

Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology 163, 161–179.
Plasticity of the Arabidopsis root system under nutrient deficiencies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVygsbjM&md5=a6fb3d011f896b0445e648056cda39e6CAS | 23852440PubMed |

Gu J, Xu Y, Dong X, Wang H, Wang Z (2014) Root diameter variations explained by anatomy and phylogeny of 50 tropical and temperate tree species. Tree Physiology 34, 415–425.
Root diameter variations explained by anatomy and phylogeny of 50 tropical and temperate tree species.Crossref | GoogleScholarGoogle Scholar | 24695727PubMed |

Heiser CBJ, Smith DM, Clevenger SB, Martin WCJ (1969) The North American sunflowers: Helianthus. Memoirs of the Torrey Botanical Club 22, 1–218.

Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162, 9–24.
The plastic plant: root responses to heterogeneous supplies of nutrients.Crossref | GoogleScholarGoogle Scholar |

Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant, Cell & Environment 22, 811–820.
Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete.Crossref | GoogleScholarGoogle Scholar |

Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA (2011) Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. Journal of Ecology 99, 954–963.
Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest.Crossref | GoogleScholarGoogle Scholar |

Hutchings MJ, de Kroon H (1994) Foraging in plants: the role of morphological plasticity in resource acquisition. Advances in Ecological Research 25, 159–238.
Foraging in plants: the role of morphological plasticity in resource acquisition.Crossref | GoogleScholarGoogle Scholar |

Jackson RB, Manwaring JH, Caldwell MM (1990) Rapid physiological adjustment of roots to localized soil enrichment. Nature 344, 58–60.
Rapid physiological adjustment of roots to localized soil enrichment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c7it1Wntw%3D%3D&md5=d5b70ef0da4675b92eb2385e6976b9fdCAS | 18278027PubMed |

James JJ, Richards JH (2006) Plant nitrogen capture in pulse-driven systems: interactions between root responses and soil processes. Journal of Ecology 94, 765–777.
Plant nitrogen capture in pulse-driven systems: interactions between root responses and soil processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsFWjsrk%3D&md5=a3a1d4d7835b0d07b39e71049cc42f0cCAS |

Kane NC, Burke JM, Marek L, Seiler G, Vear F, Baute G, Knapp SJ, Vincourt P, Rieseberg LH (2013) Sunflower genetic, genomic, and ecological resources. Molecular Ecology Resources 13, 10–20.
Sunflower genetic, genomic, and ecological resources.Crossref | GoogleScholarGoogle Scholar | 23039950PubMed |

Kellermeier F, Chardon F, Amtmann A (2013) Natural variation of Arabidopsis root architecture reveals complementing adaptive strategies to potassium starvation. Plant Physiology 161, 1421–1432.
Natural variation of Arabidopsis root architecture reveals complementing adaptive strategies to potassium starvation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvFKrurY%3D&md5=f26e50968b0a77c8c84c886fc5fbfa2dCAS | 23329148PubMed |

Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Advances in Ecological Research 23, 187–261.
Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXksVGiu7w%3D&md5=55140a0d5a30499ad326d4a2892ac4b8CAS |

Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant and Soil 334, 11–31.
Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqtbnJ&md5=fba704e737e583986ce47b5931d2dca1CAS |

Lynch JP, Brown KM (2001) Topsoil foraging – an architectural adaptation of plants to low phosphorus availability. Plant and Soil 237, 225–237.
Topsoil foraging – an architectural adaptation of plants to low phosphorus availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVWltA%3D%3D&md5=2167aeb863f02116202b790af07fc5fbCAS |

Mason CM, Donovan LA (2015) Evolution of the leaf economics spectrum in herbs: evidence from environmental divergences in leaf physiology across Helianthus (Asteraceae). Evolution 69, 2705–2720.
Evolution of the leaf economics spectrum in herbs: evidence from environmental divergences in leaf physiology across Helianthus (Asteraceae).Crossref | GoogleScholarGoogle Scholar | 26339995PubMed |

Mehlich A (1984) Mehlich III soil test extractant: a modification of Mehlich II extractant. Communications in Soil Science and Plant Analysis 15, 1409–1416.
Mehlich III soil test extractant: a modification of Mehlich II extractant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhvVChsro%3D&md5=0bf26d27a7f21df9a7d48811c7d1ae5cCAS |

Motulsky HJ, Christopoulos A (2003) ‘Fitting models to biological data using linear and nonlinear regression: a practical guide to curve fitting.’ (GraphPad Software Inc.: San Diego, CA, USA)

Nicotra AB, Babicka N, Westoby M (2002) Seedling root anatomy and morphology: an examination of ecological differentiation with rainfall using phylogenetically independent contrasts. Oecologia 130, 136–145.
Seedling root anatomy and morphology: an examination of ecological differentiation with rainfall using phylogenetically independent contrasts.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83, 553–559.
Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist 193, 30–50.
Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitVKgtr0%3D&md5=4f94785faf928e28ae06069bca02dd87CAS | 22085245PubMed |

Reich PB (2014) The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102, 275–301.
The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto.Crossref | GoogleScholarGoogle Scholar |

Reynolds HL, D’Antonio C (1996) The ecological significance of plasticity in root weight ratio in response to nitrogen: opinion. Plant and Soil 185, 75–97.
The ecological significance of plasticity in root weight ratio in response to nitrogen: opinion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntlymsg%3D%3D&md5=ef29c25831233bc7a66ef093e2ba3a50CAS |

Roumet C, Urcelay C, Díaz S (2006) Suties of root traits differ between annual and perennial species growing in the field. New Phytologist 170, 357–368.
Suties of root traits differ between annual and perennial species growing in the field.Crossref | GoogleScholarGoogle Scholar | 16608460PubMed |

Ryser P (2006) The mysterious root length. Plant and Soil 286, 1–6.
The mysterious root length.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xps1WisrY%3D&md5=b3267f2e0ce2d85f5c0f75256a5c0f9cCAS |

Ryser P, Lambers H (1995) Root and leaf attributes accounting for the performance of fast- and slow-growing grasses at different nutrient supply. Plant and Soil 170, 251–265.
Root and leaf attributes accounting for the performance of fast- and slow-growing grasses at different nutrient supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmtFOmtbs%3D&md5=5d971925eb9db3d2078a46ec715d410bCAS |

Stephens JD, Rogers WL, Mason CM, Donovan LA, Malmberg RL (2015) Species tree estimation of the genus Helianthus (Asteraceae) using target enrichment. American Journal of Botany 102, 910–920.
Species tree estimation of the genus Helianthus (Asteraceae) using target enrichment.Crossref | GoogleScholarGoogle Scholar | 26101417PubMed |

Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2013) Maize root growth angles become steeper under low N conditions. Field Crops Research 140, 18–31.
Maize root growth angles become steeper under low N conditions.Crossref | GoogleScholarGoogle Scholar |

Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, van Tienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology & Evolution 10, 212–217.
Adaptive phenotypic plasticity: consensus and controversy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFagtQ%3D%3D&md5=56e05de8314530ab81878ae78625c2aeCAS |

Wahl S, Ryser P (2000) Root tissue structure is linked to ecological strategies of grasses. New Phytologist 148, 459–471.
Root tissue structure is linked to ecological strategies of grasses.Crossref | GoogleScholarGoogle Scholar |

Wiesler F, Horst WJ (1994) Root growth and nitrate utilization of maize cultivars under field conditions. Plant and Soil 163, 267–277.
Root growth and nitrate utilization of maize cultivars under field conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXislWmt7g%3D&md5=c2829d3585f62be96eef419a0be408d2CAS |

Wright IJ, Westoby M (1999) Differences in seedling growth behavior among species: trait correlations across species, and trait shifts along nutrient compared to rainfall gradients. Journal of Ecology 87, 85–97.
Differences in seedling growth behavior among species: trait correlations across species, and trait shifts along nutrient compared to rainfall gradients.Crossref | GoogleScholarGoogle Scholar |

Wright IJ, Westoby M, Reich PB (2002) Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. Journal of Ecology 90, 534–543.
Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span.Crossref | GoogleScholarGoogle Scholar |

Zobel RW, Alloush GA, Belesky DP (2006) Differential root morphology response to no versus high phosphorus in three hydroponically grown forage chicory cultivars. Environmental and Experimental Botany 57, 201–208.
Differential root morphology response to no versus high phosphorus in three hydroponically grown forage chicory cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslSks78%3D&md5=02ff5973ce370e30e055d591d9ed5de6CAS |

Zobel RW, Kinraide TB, Baligar VC (2007) Fine root diameters can change in response to changes in nutrient concentrations. Plant and Soil 297, 243–254.
Fine root diameters can change in response to changes in nutrient concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptFegsLY%3D&md5=80553eedf50d3c63529d8a832b826ae3CAS |