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 FRONT

The utility of phenotypic plasticity of root hair length for phosphorus acquisition

Jinming Zhu A , Chaochun Zhang A B and Jonathan P. Lynch A C D
+ Author Affiliations
- Author Affiliations

A Department of Horticulture, Penn State, University Park, PA 16802, USA.

B Department of Plant Nutrition, China Agricultural University, Beijing 100193, PR China.

C Ecology Program, Penn State, University Park, PA 16802, USA.

D Corresponding author. Email: jpl4@psu.edu

Functional Plant Biology 37(4) 313-322 https://doi.org/10.1071/FP09197
Submitted: 27 July 2009  Accepted: 3 October 2009   Published: 26 March 2010

Abstract

Root hairs are subcellular protrusions from the root epidermis that are important for the acquisition of immobile nutrients such as phosphorus (P). Genetic variation exists for both root hair length and the plasticity of root hair length in response to P availability, where plasticity manifests as increased root hair length in response to low P availability. Although it is known that long root hairs assist P acquisition, the utility of phenotypic plasticity for this trait is not known. To assess the utility of root hair plasticity for adaptation to low phosphorus availability, we evaluated six recombinant inbred lines of maize (Zea mays L.) with varying root hair lengths and root hair plasticity in a controlled environment and in the field. Genotypes with long root hairs under low P availability had significantly greater plant growth, P uptake, specific P absorption rates and lower metabolic cost-benefit ratios than short-haired genotypes. Root hair length had no direct effect on root respiration. In the controlled environment, plastic genotypes had greater biomass allocation to roots, greater reduction in specific root respiration and greater final biomass accumulation at low phosphorus availability than constitutively long-haired genotypes. In the field study, the growth of plastic and long-haired genotypes were comparable under low P, but both were superior to short-haired genotypes. We propose that root hair plasticity is a component of a broader suite of traits, including plasticity in root respiration, that permit greater root growth and phosphorus acquisition in low P soils.

Additional keywords: phosphate, root hairs, Zea mays.


Acknowledgements

We thank Kathleen Brown and Richard Craig for helpful discussions and Shawn Kaeppler at the University of Wisconsin for providing seeds. This research was supported by USDA-NRI grant 00353009246 to Shawn Kaeppler and JPL and NSF grant 0135872 to JPL and Kathleen Brown.


References


Anonymous (1887) Report of the Pennsylvania State College Agricultural Experimental Station. Official Document Number 13.

Atkinson D (1973) Some general effects of phosphorus deficiency on growth and development. New Phytologist 72, 101–111.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Barber SA (1995) ‘Soil nutrient bioavailability: a mechanistic approach.’ (Wiley & Sons Inc.: New York)

Bates TR (1998) The importance of root hairs in phosphorus acquisition and the mechanism of root hair elongation in phosphorus deficient Arabidopsis thaliana plants. PhD Thesis. The Pennsylvania State University, University Park, Pennsylvania, PA, USA.

Bates T, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant, Cell & Environment 19, 529–538.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bates TR, Lynch JP (2000a) Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana. American Journal of Botany 87, 958–963.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Bates TR, Lynch JP (2000b) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. American Journal of Botany 87, 964–970.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant and Soil 236, 243–250.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bhat KKS, Nye PH (1974) Diffusion of phosphate to plant roots in soil III. Depletion around onion roots without root hairs. Plant and Soil 41, 383–394.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bloom AJ, Chapin FSI, Mooney HA (1985) Resource limitation in plants – an economic analogy. Annual Review of Ecology and Systematics 16, 363–392. open url image1

Bouldin DR (1961) Mathematical description of diffusion process in the soil. Soil Science Society of America Proceedings 25, 476–480.
CAS |
open url image1

Bouma TJ, Nielsen KL, Eissenstat DM, Lynch JP (1997a) Soil CO2 concentration does not affect growth or root respiration in bean or citrus. Plant, Cell & Environment 20, 1495–1505.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bouma TJ, Nielsen KL, Eissenstat DM, Lynch JP (1997b) Estimating respiration of roots in soil: interactions with soil CO2, soil temperature and soil water content. Plant and Soil 195, 221–232.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Brouwer R (1962) Nutritive influences on the distribution of dry matter in the plant. Netherlands Journal of Agricultural Science 10, 399–408. open url image1

Brouwer R (1983) Functional equilibrium: sense or nonsense? Netherlands Journal of Agricultural Science 31, 335–348. open url image1

Caradus JR (1981) Effect of root hair length on white clover growth over a range of soil phosphorus levels. NZ. Journal of Agricultural Research 24, 359–364. open url image1

Ciereszko I, Gniazdowska A, Mikulska M, Rychter AM (1996) Assimilate translocation in bean plants (Phaseolus vulgaris L.) during phosphate deficiency. Journal of Plant Physiology 149, 343–348.
CAS |
open url image1

Clarkson DT (1985) Factors affecting mineral nutrient acquisition by plants. Annual Review of Plant Physiology 36, 77–115.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Clarkson DT, Carvajal M, Henzler T, Waterhouse RN, Smyth AJ, Cooke DT (2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. Journal of Experimental Botany 51, 61–70.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

DaSilva AE , Gabelman WH (1993) Screening maize inbred lines for tolerance to low P stress conditions. In ‘Genetic aspects of plant mineral nutrition’. (Eds PJ Randall, E Delhaize, RA Richards and R Munns) pp. 233–239. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Fan M, Zhu J, Richards C, Brown K, Lynch JP (2003) Physiological roles for aerenchyma in phosphorus-stressed roots. Functional Plant Biology 30, 493–506.
Crossref | GoogleScholarGoogle Scholar | open url image1

Foehse D, Jungk A (1983) Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Plant and Soil 74, 359–368.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Foehse D, Claassen N, Jungk A (1991) Phosphorus efficiency of plants. II Significance of root radius, root hairs and cation–anion balance for phosphorus influx in seven plant species. Plant and Soil 132, 261–272.
CAS |
open url image1

Gahoonia TS, Nielsen NE (1997) Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98, 177–182.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (32P) uptake from soil. Plant and Soil 198, 147–152.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gahoonia TS, Nielsen NE (2003) Phosphorus uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low and high phosphorus soils. Plant, Cell & Environment 26, 1759–1766.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gahoonia TS, Care D, Nielsen NE (1997) Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant and Soil 191, 181–188.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gahoonia TS, Nielsen NE, Lyshede OB (1999) Phosphorus acquisition of cereal cultivars in the field at three levels of phosphorus fertilization. Plant and Soil 211, 269–281.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001) A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake. Plant and Soil 235, 211–219.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Green RL, Beard JB, Oprisko MJ (1991) Root hairs and root lengths in nine warm-season turfgrass genotypes. Journal of the American Society for Horticultural Science 116, 965–969. open url image1

Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant and Soil 237, 173–195.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Hood ME, Shew HD (1997) Initial cellular interactions between Thielaviopsis basicola and tobacco root hairs. Phytopathology 87, 228–235.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hunt R (1975) Further observations on root-shoot equilibrium in perennial ryegrass (Lolium perenne L.). Annals of Botany 39, 745–755. open url image1

Hunt R (1990) ‘Basic growth analysis.’ (Unwin Hyman Ltd: London)

Itoh S, Barber S (1983a) A numerical solution of whole plant nutrient uptake for soil root systems with root hairs. Plant and Soil 70, 403–413.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Itoh S, Barber S (1983b) Phosphorus uptake by six plant species as related to root hairs. Agronomy Journal 75, 457–461. open url image1

Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. Journal of Plant Nutrition and Soil Science 164, 121–129.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kaeppler SM, Parke JL, Mueller SM, Senior L, Stuber C, Tracy WF (2000) Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Science 40, 358–364. open url image1

Koide R, Elliott G (1989) Cost, benefit and efficiency of the vesicular-arbuscular mycorrhizal symbiosis. Functional Ecology 3, 252–255. open url image1

Koide RT, Goff MD, Dickie IA (2000) Component growth efficiencies of mycorrhizal and nonmycorrhizal plants. New Phytologist 148, 163–168.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lambers H , Atkin OK , Millenaar FF (2002) Respiratory patterns in roots in relation to their functioning. In ‘The hidden half’. 3rd edn. (Eds A Eshel, U Kafkaki) pp. 521–552. (Marcel Dekker Inc.: New York)

Lewis DG, Quirk JP (1967) Phosphate diffusion in soil and uptake by plants. Plant and Soil 26, 445–453.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lynch JP (1998) The role of nutrient efficient crops in modern agriculture. Journal of Crop Production 1, 241–264.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lynch JP (2007) Roots of the second green revolution. Australian Journal of Botany 55, 493–512.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lynch JP , Brown KM (2006) Whole plant adaptations to low phosphorus availability. In ‘Plant–environment interactions’. 3rd edn. (Ed. B Huang) pp. 209–242. (Taylor & Francis: New York)

Lynch JP , Deikman J (1998) Phosphorus in plant biology: regulatory roles in molecular, cellular, organismic, and ecosystem processes. In ‘Current topics in plant physiology: an American Society of Plant Physiologists Series. Vol. 19’. (American Society of Plant Physiologists: Rockville, MD)

Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269, 45–56.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lynch JP, Epstein E, Lauchli A, Weigt GE (1990) An automated greenhouse sand culture system suitable for studies of phosphorus nutrition. Plant, Cell & Environment 13, 547–554.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lynch JP, Lauchli A, Epstein E (1991) Vegetative growth of common bean in response to phosphorus nutrition. Crop Science 31, 380–387.
CAS |
open url image1

Ma Z, Walk TC, Marcus A, Lynch JP (2001a) Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach. Plant and Soil 236, 221–235.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001b) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant, Cell & Environment 24, 459–467.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Miguel M (2004) Genotypic variation in root hairs and phosphorus efficiency in common bean (Phaseolus vulgaris L.). In ‘Horticulture’. (Pennsylvania State University: University Park, PA)

Mollier A, Pellerin S (1999) Maize root system growth and development as influenced by phosphorus deficiency. Journal of Experimental Botany 50, 487–497.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Murphy J, Riley J (1962) A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27, 31–36.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Nielsen NE, Barber SA (1978) Differences among genotypes of corn in the kinetics of phosphorus uptake. Agronomy Journal 70, 695–698.
CAS |
open url image1

Nielsen KL, Bouma TJ, Lynch JP, Eissenstat DM (1998) Effects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris). New Phytologist 139, 647–656.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nielsen KL, Eshel A, Lynch JP (2001) The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes. Journal of Experimental Botany 52, 329–339.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Peterson RL, Farquhar ML (1996) Root hairs: specialized tubular cells extending root surfaces. Botanical Review 62, 1–40.
Crossref | GoogleScholarGoogle Scholar | open url image1

Radin JW, Eidenbrock MP (1984) Hydraulic conductance as a factor limiting leaf expansion of phosphorus deficient soybean plants. Plant Physiology 75, 372–377.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rubio G, Zhu J, Lynch JP (2003) A critical test of two prevailing theories of plant response to nutrient availability. American Journal of Botany 90, 143–152.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology and Plant Molecular Biology 52, 527–560.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Salama AD, Waring PF (1979) Effects of mineral nutrition on endogenous cytokinins in plants of sunflower (Helianthus annuus L.). Journal of Experimental Botany 30, 971–981.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Sample EC , Soper RJ , Racz GJ (1980) Reactions of phosphate fertilizers in soils. In ‘The role of phosphorus in agriculture’. (Eds FE Khasawneh, EC Sample, EJ Kamprath) pp. 263–310. (American Society of Agronomy: Madison, WI)

Senior ML, Chin ECL, Lee M, Smith JSC, Stuber CW (1996) Simple sequence repeat markers developed from maize sequences found in Genbank database: map construction. Crop Science 36, 1676–1683.
CAS |
open url image1

Snapp S, Koide R, Lynch J (1995) Exploitation of localized phosphorus patches by common bean roots. Plant and Soil 177, 211–218.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Taylor HM (1987) ‘Minirhizotron observation tubes: methods and applications for measuring rhizophere dynamics.’ (American society of Agronomy: New Orleans)

Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 157, 423–447.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Walk T, Jaramillo R, Lynch J (2006) Architectural tradeoffs between adventitious and basal roots for phosphorus acquisition. Plant and Soil 279, 347–366.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Wang L, Liao H, Yan X, Zhuang B, Dong Y (2004) Genetic variability for root hair traits as related to phosphorus status in soybean. Plant and Soil 261, 77–84.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Wen TJ, Schnable PS (1994) Analysis of mutant of three genes that influence root hair development in Zea mays (Graminae) suggest that root hairs are dispensable. American Journal of Botany 81, 833–842.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yan XL, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant and Soil 265, 17–29.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Zhang YJ, Lynch JP, Brown KM (2003) Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. Journal of Experimental Botany 54, 2351–2361.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Zhu J (2003) Composite interval mapping and physiological function of root traits conferring phosphorus efficiency in maize (Zea mays L.). PhD Thesis. The Pennsylvania State University, University Park, PA, USA.

Zhu J, Lynch J (2004) The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays L.) seedlings. Functional Plant Biology 31, 949–958.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Zhu J, Kaeppler SM, Lynch JP (2005a) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant and Soil 270, 299–310.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Zhu J, Kaeppler SM, Lynch JP (2005b) Topsoil foraging and phosphorus acquisition efficiency in maize (Zea mays L.). Functional Plant Biology 32, 749–762.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Zhu J, Kaeppler SM, Lynch JP (2005c) Mapping of QTL for lateral root branching and length in maize (Zea mays) under differential phosphorus supply. Theoretical and Applied Genetics 111, 688–695.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Zhu J, Mickelson SM, Kaeppler SM, Lynch JP (2006) Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels. Theoretical and Applied Genetics 113, 1–10.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1