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Plant function and evolutionary biology
RESEARCH ARTICLE

Ethylene modulates genetic, positional, and nutritional regulation of root plagiogravitropism

Paramita Basu A , Yuan-Ji Zhang B , Jonathan P. Lynch A B and Kathleen M. Brown A B C
+ Author Affiliations
- Author Affiliations

A Intercollege Program in Plant Biology, The Pennsylvania State University, University Park, PA 16802, USA.

B Department of Horticulture, The Pennsylvania State University, University Park, PA 16802, USA.

C Corresponding author. Email: kbe@psu.edu

Functional Plant Biology 34(1) 41-51 https://doi.org/10.1071/FP06209
Submitted: 30 August 2006  Accepted: 17 November 2006   Published: 19 January 2007

Abstract

Plagiogravitropic growth of roots strongly affects root architecture and topsoil exploration, which are important for the acquisition of water and nutrients. Here we show that basal roots of Phaseolus vulgaris L. develop from 2–3 definable whorls at the root–shoot interface and exhibit position-dependent plagiogravitropic growth. The whorl closest to the shoot produces the shallowest roots, and lower whorls produce deeper roots. Genotypes vary in both the average growth angles of roots within whorls and the range of growth angles, i.e. the difference between the shallowest and deepest basal roots within a root system. Since ethylene has been implicated in both gravitropic and edaphic stress responses, we studied the role of ethylene and its interaction with phosphorus availability in regulating growth angles of genotypes with shallow or deep basal roots. There was a weak correlation between growth angle and ethylene production in the basal rooting zone, but ethylene sensitivity was strongly correlated with growth angle. Basal roots emerging from the uppermost whorl were more responsive to ethylene treatment than the lower-most whorl, displaying shallower angles and inhibition of growth. Ethylene sensitivity is greater for shallow than for deep genotypes and for plants grown with low phosphorus compared with those supplied with high phosphorus. Ethylene exposure increased the range of angles, although deep genotypes grown in low phosphorus were less affected. Our results identify basal root whorl number as a novel architectural trait, and show that ethylene mediates regulation of growth angle by position of origin, genotype and phosphorus availability.

Additional keywords: basal roots, gravitropism, Phaseolus vulgaris, phosphorus, root architecture.


Acknowledgements

The authors gratefully acknowledge support from US-AID Bean-Cowpea CRSP.


References


Abeles FB , Morgan PW , Saltveit ME (1992) ‘Ethylene in plant biology.’ (Academic Press Inc.: San Diego)

Arshad M , Frankenberger WTJ (2002) ‘Ethylene: agricultural sources and applications.’ (Kluwer Academic: New York)

Beebe S, Lynch J, Galwey N, Tohme J, Ochoa I (1997) A geographical approach to identify phosphorus-efficient genotypes among landraces and wild ancestors of common bean. Euphytica 95, 325–336.
Crossref | GoogleScholarGoogle Scholar | open url image1

Beyer E (1973) Abscission: support for a role of ethylene modification of auxin transport. Plant Physiology 52, 1–5.
PubMed |
open url image1

Blancaflor EB, Masson PH (2003) Plant gravitropism. Unraveling the ups and downs of a complex process. Plant Physiology 133, 1677–1690.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bonser AM, Lynch J, Snapp S (1996) Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytologist 132, 281–288.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boonsirichai K, Guan C, Chen R, Masson PH (2002) Root gravitropism: an experimental tool to investigate basic cellular and molecular processes underlying mechanosensing and signal transmission in plants. Annual Review of Plant Biology 53, 421–447.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Borch K, Bouma TJ, Lynch JP, Brown KM (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant, Cell and Environment 22, 425–431.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiology 126, 524–535.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Buer CS, Sukumar P, Muday GK (2006) Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiology 140, 1384–1396.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Campbell RB, Moreau RA (1979) Ethylene in a compacted field soil and its effect on growth, tuber quality and yield of potatoes. American Potato Journal 56, 199–210. open url image1

De Paepe A, Vuylsteke M, Van Hummelen P, Zabeau M, Van Der Straeten D (2004) Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis. The Plant Journal 39, 537–559.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Edelmann HG (2002) Ethylene perception generates gravicompetence in gravi-incompetent leaves of rye seedlings. Journal of Experimental Botany 53, 1825–1828.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Edelmann HG, Gudi G, Kuhnemann F (2002) The gravitropic setpoint angle of dark-grown rye seedlings and the role of ethylene. Journal of Experimental Botany 53, 1627–1634.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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

Frahm MA, Rosas JC, Mayek-Perez N, Lopez-Salinas E, Acosta-Gallegos JA, Kelly JD (2004) Breeding beans for resistance to terminal drought in the lowland tropics. Euphytica 136, 223–232.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ge Z, Rubio G, Lynch JP (2000) The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant and Soil 218, 159–171.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Guisinger M, Kiss J (1999) The influence of microgravity and spaceflight on columella cell ultrastructure in starch-deficient mutants of Arabidopsis. American Journal of Botany 86, 1357–1366.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. The Plant Cell 12, 757–770.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

He CJ, Morgan PW, Drew MC (1992) Enhanced sensitivity to ethylene in nitrogen-starved or phosphate-starved roots of Zea mays L. during aerenchyma formation. Plant Physiology 98, 137–142.
PubMed |
open url image1

Ho MD, McCannon BC, Lynch JP (2004) Optimization modeling of plant architecture for water and phosphorus acquisition. Journal of Theoretical Biology 226, 331–340.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ho MD, Rosas JC, Brown KM, Lynch JP (2005) Root architectural tradeoffs for water and phosphorus acquisition. Functional Plant Biology 32, 737–748.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jacobs M, Rubery PH (1988) Naturally occurring auxin transport regulators. Science 241, 346–349.
Crossref | GoogleScholarGoogle Scholar | open url image1

LaMotte CE, Pickard BG (2004) Control of gravitropic orientation. II. Dual receptor model for gravitropism. Functional Plant Biology 31, 109–120.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lee JS, Chang W, Evans ML (1990) Effects of ethylene on the kinetics of curvature and auxin redistribution in gravistimulated roots of Zea mays. Plant Physiology 94, 1770–1775.
PubMed |
open url image1

Liao H, Rubio G, Yan XL, Cao AQ, Brown KM, Lynch JP (2001) Effect of phosphorus availability on basal root shallowness in common bean. Plant and Soil 232, 69–79.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liao H, Yan XL, Rubio G, Beebe SE, Blair MW, Lynch JP (2004) Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Functional Plant Biology 31, 959–970.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lynch J (2006) Roots of the second green revolution. Australian Journal of Botany , open url image1

Lynch J, Brown KM (1997) Ethylene and plant responses to nutritional stress. Physiologia Plantarum 100, 613–619.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lynch J, van Beem JJ (1993) Growth and architecture of seedling roots of common bean genotypes. Crop Science 33, 1253–1257. open url image1

Lynch JP (1995) Root architecture and plant productivity. Plant Physiology 109, 7–13.
PubMed |
open url image1

Lynch JP, Brown KM (2001) Topsoil foraging – an architectural adaptation of plants to low phosphorus availability. Plant and Soil 237, 225–237.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiology 131, 1381–1390.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Madlung A, Behringer FJ, Lomax TL (1999) Ethylene plays multiple nonprimary roles in modulating the gravitropic response in tomato. Plant Physiology 120, 897–906.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Murphy A, Peer WA, Taiz L (2000) Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211, 315–324.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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

Perrin RM, Young L-S, Narayana Murthy UM, Harrison BR, Wang YAN, Will JL, Masson PH (2005) Gravity signal transduction in primary roots. Annals of Botany 96, 737–743.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Philosoph-Hadas S, Meir S, Rosenberger I, Halevy AH (1996) Regulation of the gravitropic response and ethylene biosynthesis in gravistimulated snapdragon spikes by calcium chelators and ethylene inhibitors. Plant Physiology 110, 301–310.
PubMed |
open url image1

Ponce G, Barlow PW, Feldman LJ, Cassab GI (2005) Auxin and ethylene interactions control mitotic activity of the quiescent centre, root cap size, and pattern of cap cell differentiation in maize. Plant, Cell and Environment 28, 719–732.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pothuluri J, Kissel D, Whitney D, Thien S (1986) Phosphorus uptake from soil layers having different soil test phosphorus levels. Agronomy Journal 78, 991–994. open url image1

Rubio G, Liao H, Yan XL, Lynch JP (2003) Topsoil foraging and its role in plant competitiveness for phosphorus in common bean. Crop Science 43, 598–607. open url image1

Rubio G, Walk T, Ge ZY, Yan XL, Liao H, Lynch JP (2001) Root gravitropism and below-ground competition among neighbouring plants: a modelling approach. Annals of Botany 88, 929–940.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sanyal D, Bangerth F (1998) Stress induced ethylene evolution and its possible relationship to auxin-transport, cytokinin levels, and flower bud induction in shoots of apple seedlings and bearing apple trees. Plant Growth Regulation 24, 127–134.
Crossref | GoogleScholarGoogle Scholar | open url image1

Singh SP (1982) A key for identification of different growth habits of Phaseolus vulgaris L. Annual Report of the Bean Improvement Cooperative 25, 92–95. open url image1

Singh SP, Gepts P, Debouck DG (1991) Races of common bean (Phaseolus vulgaris, Fabaceae). Economic Botany 45, 379–396. open url image1

Suttle JC (1988) Effect of ethylene treatment on polar IAA transport, net IAA uptake and specific binding of N-1-naphthylphthalamic acid in tissues and microsomes isolated from etiolated pea epicotyls. Plant Physiology 88, 795–799.
PubMed |
open url image1

Yan X, Beebe SE, Lynch JP (1995) Genetic variation for phosphorus efficiency of common bean in contrasting soil types: II. Yield response. Crop Science 35, 1094–1099. open url image1

Zhang YJ (2002) Ethylene and phosphorus responses in plants. PhD thesis, Pennsylvania State University, PA.

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 | PubMed | open url image1

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

Zobel RW (1986) Rhizogenetics (root genetics) of vegetable crops. HortScience 21, 956–959. open url image1