Abstract
Background and aims
Previous research has suggested that root cortical aerenchyma (RCA) can enhance soil exploration and crop performance by decreasing root respiration. This trait is a potential breeding target for adaptation to abiotic stresses such as drought and low nutrient availability. However, little is known of phenotypic variation in aerenchyma or its distribution among root classes.
Methods
The spatial distribution of RCA was evaluated in freehand sections from 13 sites in the root systems of 11 recombinant inbred and commercial lines of maize (Zea mays). RCA variation was evaluated in 583 recombinant inbred lines of maize at one sampling position.
Results
RCA varied significantly among root classes and axial positions. Genotypic differences were observed for the amount of RCA at corresponding sampling locations and for the mean amount of RCA across all sampling locations, but genotypes did not differ in the proportional distribution of RCA within the whole root system. The amount of RCA in a cross-section was independent of several other anatomical traits.
Conclusions
There is substantial genetic variation for RCA, and this variation is independent of other anatomical traits. RCA can be phenotyped in greenhouse-grown plants by sampling the middle parts of second- or third-whorl crown roots.
Similar content being viewed by others
Abbreviations
- RCA:
-
Root cortical aerenchyma
References
Araus JL, Slafer GA, Royo C, Serret MD (2008) Breeding for yield potential and stress adaptation in cereals. Crit Rev Plant Sci 27:377–412
Armstrong W (1972) Re-examination of the functional significance of aerenchyma. Physiol Plant 27:173–177
Bailey-Serres J, Voesenek L (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339
Bouranis DL, Chorianopoulou SN, Siyiannis VF, Protonotarios VE, Hawkesford MJ (2003) Aerenchyma formation in roots of maize during sulphate starvation. Planta 217:382–391
Bouranis DL, Chorianopoulou SN, Kollias C, Maniou P, Protonotarios VE, Siyiannis VF, Hawkesford MJ (2006) Dynamics of aerenchyma distribution in the cortex of sulfate-deprived adventitious roots of maize. Ann Bot 97:695–704
Burton AL (2010) Genetic basis and high throughput phenotypic evaluation of anatomical and architectural root traits for resource acquisition in Zea mays. PhD dissertation, The Pennsylvania State University, USA
Burton AL, Lynch JP, Brown KM (2012) RootScan: software for high-throughput analysis of root anatomical traits. Plant Soil 357:189–203
Colmer TD (2003a) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Ann Bot 91:301–309
Colmer TD (2003b) Long distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17–36
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
Doussan C, Pagès L, Pierret A (2003) Soil exploration and resource acquisition by plant roots: an architectural and modelling point of view. Agronomie 23:419–431
Drew MC (1994) Nutrient uptake by roots of cereals in oxygen deficient environment. In: Singh VP, Singh RK, Singh BB, Zeigler RS (eds) Physiology of stress tolerance in rice. Proceedings, IRRI, Los Banos, Philippines, pp 70–79
Drew MC, Saker LR (1978) Nutrient supply and the growth of the seminal root system in barley. J Exp Bot 29:435–451
Drew MC, Jackson M, Giffard S (1979) Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) in roots may be adaptive responses to flooding Zea mays L. Planta 147:83–88
Drew M, He C, Morgan P (1989) Decreased ethylene biosynthesis, and induction of aerenchyma, by nitrogen- or phosphate-starvation in adventitious roots of Zea mays L. Plant Physiol 91:266–271
Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782
Esau K (1977) Anatomy of seed plants, 2nd edn. John Wiley and Sons, New York
Evans DE (2004) Aerenchyma formation. New Phytol 161:35–49
Fan MS, Zhu JM, Richards C, Brown KM, Lynch JP (2003) Physiological roles for aerenchyma in phosphorus-stressed roots. Funct Plant Biol 30:493–506
Garthwaite AJ, von Bothmer R, Colmer TD (2003) Diversity in root aeration traits associated with waterlogging tolerance in the genus Hordeum. Funct Plant Biol 30:875–889
Gregory PJ (2006) Plant roots: growth, activity and interaction with soils. Blackwell Publishing, Oxford
Gregory PJ, Bengough AG, Grinev D, Schmidt S, Thomas WTB, Wojciechowski T, Young IM (2009) Root phenomics of crops: opportunities and challenges. Funct Plant Biol 36:922–929
Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001a) Characterization of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212:205–214
Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001b) Rapid changes in cell wall pectic polysaccharides are closely associated with early stages of aerenchyma formation, a spatially localized form of programmed cell death in roots of maize (Zea mays L.) promoted by ethylene. Plant Cell Environ 24:1369–1375
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 Physiol 98:137–142
Ho MD, Rosas JC, Brown KM, Lynch JP (2005) Root architectural tradeoffs for water and phosphorus acquisition. Funct Plant Biol 32:737–748
Hochholdinger F (2009) The maize root system: morphology, anatomy and genetics. In: Bennetzen JL, Hake SC (eds) Handbook of maize: its biology. Springer Science and Business Media, New York, pp 145–160
Jackson MB, Fenning TM, Jenkins W (1985) Aerenchyma (gas space) formation in adventitious roots of rice (Oryza sativa L.) is not controlled by ethylene or small partial pressures of oxygen. J Exp Bot 36:1566–1572
Justin S, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytol 106:465–495
Kawai M, Samarajeewa PK, Barrero RA, Nishiguchi M, Uchimiya H (1998) Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots. Planta 204:277–287
Konings H (1982) Ethylene-promoted formation of aerenchyma in seedling roots of Zea mays L. under aerated and non-aerated conditions. Physiol Plant 54:119–124
Konings H, Verschuren G (1980) Formation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to nutrient supply. Physiol Plant 49:265–279
Lenochova Z, Soukup A, Votrubova O (2009) Aerenchyma formation in maize roots. Biol Plant 53:263–270
Liljeroth E (1995) Comparisons of early root cortical senescence between barley cultivars, triticum species and other cereals. New Phytol 130:495–501
Lu Y, Wassmann R, Neue HU, Huang C (1999) Impact of phosphorus supply on root exudation, aerenchyma formation and methane emission of rice plants. Biogeochemistry 47:203–218
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049
Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56
Mano Y, Omori F (2007) Breeding for flooding tolerant maize using “teosinte” as a germplasm resource. Plant Root 1:17–21
Mano Y, Omori F, Takamizo T, Kindiger B, Bird RM, Loaisiga CH (2006) Variation for root aerenchyma formation in flooded and non-flooded maize and teosinte seedlings. Plant Soil 281:269–279
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, San Diego
Peterson CA, Perumalla CJ (1984) Development of the hypodermal casparian band in corn and onion roots. J Exp Bot 35:51–57
Postma JA, Lynch JP (2011a) Root cortical aerenchyma enhances growth of Zea mays L. on soils with suboptimal availability of nitrogen, phosphorus and potassium. Plant Physiol 156:1190–1201
Postma JA, Lynch JP (2011b) Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability. Ann Bot 107:829–841
Ray JD, Kindiger B, Dewald CL, Sinclair TR (1998) Preliminary survey of root aerenchyma in Tripsacum. Maydica 43:49–53
Reynolds M, Manes Y, Izanloo A, Langridge P (2009) Phenotyping approaches for physiological breeding and gene discovery in wheat. Ann Appl Biol 155:309–320
Richards RA (2006) Physiological traits used in breeding of new cultivars for water-scarce environments. Agr Water Manag 80:197–211
Saab IN, Sachs MM (1996) A flooding-induced xyloglucan endo-transglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma. Plant Physiol 112:385–391
Sinclair T (2011) Challenges in breeding for yield increase for drought. Trends Plant Sci 16:289–293
Siyiannis VF, Protonotarios VE, Zechmann B, Chorianopoulou SN, Müller M, Hawkesford MJ, Bouranis DL (2011) Comparative spatiotemporal analysis of root aerenchyma formation processes in maize due to sulphate, nitrate or phosphate deprivation. Protoplasma 249:671–686
Steudle E, Peterson CA (1998) How does water get through roots? J Exp Bot 49:775–788
Striker GG, Insausti P, Grimoldi AA, Vega AS (2007) Trade-off between root porosity and mechanical strength in species with different types of aerenchyma. Plant Cell Environ 30:580–589
Tombesi S, Johnson RS, Day KR, DeJong TM (2010) Relationships between xylem vessel characteristics, calculated axial hydraulic conductance and size-controlling capacity of peach rootstocks. Ann Bot 105:327–331
Umantha S (2001) Expression of expansins in relation to the development of aerenchyma in the primary root of Zea mays, MS Thesis, The Pennsylvania State University, United States
Zaidi PH, Mani Selvan P, Sultana R, Srivastava A, Singh AK, Srinivasan G, Singh RP, Singh PP (2007) Association between line per se and hybrid performance under excessive soil moisture stress in tropical maize (Zea mays L.). Field Crop Res 101:117–126
Zhu JM, Brown KM, Lynch JP (2010) Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). Plant Cell Environ 33:740–749
Acknowledgments
We thank Lauren Gelesh, Johanna Mirenda and Robert Snyder for technical assistance. This work was supported by the United States Department of Agriculture National Research Initiative grant # 207-35100-18365 to JPL and KMB.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Peter J. Gregory.
Rights and permissions
About this article
Cite this article
Burton, A.L., Lynch, J.P. & Brown, K.M. Spatial distribution and phenotypic variation in root cortical aerenchyma of maize (Zea mays L.). Plant Soil 367, 263–274 (2013). https://doi.org/10.1007/s11104-012-1453-7
Received:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1007/s11104-012-1453-7