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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Phenotyping for drought tolerance in grain crops: when is it useful to breeders?

J. B. Passioura
+ Author Affiliations
- Author Affiliations

CSIRO Plant Industry, PO Box 1600, Canberra, ACT 2601, Australia. Email: john.passioura@csiro.au

Functional Plant Biology 39(11) 851-859 https://doi.org/10.1071/FP12079
Submitted: 13 April 2012  Accepted: 5 September 2012   Published: 25 September 2012

Abstract

Breeding for drought tolerance in grain crops is not a generic issue. Periods of drought vary in length, timing and intensity and different traits are important with different types of drought. The search for generic drought tolerance using single-gene transformations has been disappointing. It has typically concentrated on survival of plants suffering from severe water stress, which is rarely an important trait in crops. More promising approaches that target complex traits tailored to specific requirements at the different main stages of the life of a crop, during: establishment, vegetative development, floral development and grain growth are outlined. The challenge is to devise inexpensive and effective ways of identifying promising phenotypes with the aim of aligning them with genomic information to identify molecular markers useful to breeders. Controlled environments offer the stability to search for attractive phenotypes or genotypes in a specific type of drought. The recent availability of robots for measuring large number of plants means that large numbers of genotypes can be readily phenotyped. However, controlled environments differ greatly from those in the field. Devising pot experiments that cater for important yield-determining processes in the field is difficult, especially when water is limiting. Thus, breeders are unlikely to take much notice of research in controlled environments unless the worth of specific traits has been demonstrated in the field. An essential link in translating laboratory research to the field is the development of novel genotypes that incorporate gene(s) expressing a promising trait into breeding lines that are adapted to target field environments. Only if the novel genotypes perform well in the field are they likely to gain the interest of breeders. High throughput phenotyping will play a pivotal role in this process.

Additional keywords: deficit watering, floral resilience, germplasm, prebreeding, trait, water stress.


References

Araus JL, Slafer GA, Royo C, Dolores Serret M (2008) Breeding for yield potential and stress adaptation in cereals. Critical Reviews in Plant Sciences 27, 377–412.
Breeding for yield potential and stress adaptation in cereals.Crossref | GoogleScholarGoogle Scholar |

Bänziger M, Setimela PS, Hodson D, Vivek B (2006) Breeding for improved abiotic stress tolerance in maize adapted to southern Africa. Agricultural Water Management 80, 212–224.
Breeding for improved abiotic stress tolerance in maize adapted to southern Africa.Crossref | GoogleScholarGoogle Scholar |

Bidinger F, Musgrave RB, Fischer RA (1977) Contribution of stored pre-anthesis assimilate to grain yield in wheat and barley. Nature 270, 431–433.
Contribution of stored pre-anthesis assimilate to grain yield in wheat and barley.Crossref | GoogleScholarGoogle Scholar |

Blum A (1998) Improving wheat grain filling under stress by stem reserve mobilisation. Euphytica 100, 77–83.
Improving wheat grain filling under stress by stem reserve mobilisation.Crossref | GoogleScholarGoogle Scholar |

Boyer JS, McLaughlin JE (2007) Functional reversion to identify controlling genes in multigenic responses: analysis of floral abortion. Journal of Experimental Botany 58, 267–277.
Functional reversion to identify controlling genes in multigenic responses: analysis of floral abortion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlOlt7o%3D&md5=f5c4ec5f1eac59db7f0cf1a0e4d513acCAS |

Burgueño J, de los Campos G, Weigel K, Crossa J (2012) Genomic prediction of breeding values when modeling genotype × environment interaction using pedigree and dense molecular markers. Crop Science 52, 707–719.
Genomic prediction of breeding values when modeling genotype × environment interaction using pedigree and dense molecular markers.Crossref | GoogleScholarGoogle Scholar |

Cabrera-Bosquet L, Crossa J, von Zitzewitz J, Serret MD, Araus JL (2012) High-throughput phenotyping and genomic selection: the frontiers of crop breeding converge. Journal of Integrative Plant Biology 54, 312–320.
High-throughput phenotyping and genomic selection: the frontiers of crop breeding converge.Crossref | GoogleScholarGoogle Scholar |

Campos H, Cooper A, Habben JE, Edmeades GO, Schussler JR (2004) Improving drought tolerance in maize: a view from industry. Field Crops Research 90, 19–34.
Improving drought tolerance in maize: a view from industry.Crossref | GoogleScholarGoogle Scholar |

Campos H, Cooper M, Edmeades GO, Loffler C, Schussler JR, Ibanez M (2006) Changes in drought tolerance in maize associated with fifty years of breeding for yield in the US corn belt. Maydica 51, 369–381.

Castiglioni P, Warner D, Bensen RJ, Anstrom DC, Harrison J, Stoecker M, Abad M, Kumar G, Salvador S, D’Ordine R, Navarro S, Back S, Fernandes M, Targolli J, Dasgupta S, Bonin C, Luethy MH, Heard JE (2008) Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions. Plant Physiology 147, 446–455.
Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVyhsb4%3D&md5=66fc34a65011e8df3f6cd60eb7f5216cCAS |

Chen A, Gusta LV, Brule-Babel A, Leach R, Baumann U, Fincher GB, Collins NC (2009) Varietal and chromosome 2H locus-specific frost tolerance in reproductive tissues of barley (Hordeum vulgare L.) detected using a frost simulation chamber. Theoretical and Applied Genetics 119, 685–694.
Varietal and chromosome 2H locus-specific frost tolerance in reproductive tissues of barley (Hordeum vulgare L.) detected using a frost simulation chamber.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsVejtbc%3D&md5=c0ba994126a20ce35857241abfdd8abfCAS |

Chenu K, Cooper M, Hammer GL, Mathews KL, Dreccer MF, Chapman SC (2011) Environment characterization as an aid to wheat improvement: interpreting genotype-environment interactions by modelling water-deficit patterns in north-eastern Australia. Journal of Experimental Botany 62, 1743–1755.
Environment characterization as an aid to wheat improvement: interpreting genotype-environment interactions by modelling water-deficit patterns in north-eastern Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsFyis7w%3D&md5=dedf9405c7a480df9e2c418f15da7466CAS |

Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. Journal of Experimental Botany 55, 2447–2460.
Breeding for high water-use efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVOisrk%3D&md5=9fac3d5e455da4be2a073e101a3ba619CAS |

Davies WJ, Wilkinson S, Loveys B (2002) Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture. New Phytologist 153, 449–460.
Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Wgt7Y%3D&md5=e8e28bb02dc32692b9f6a42f1ff3594dCAS |

Dolferus R, Ji X, Richards RA (2011) Abiotic stress and control of grain number in cereals. Plant Science 181, 331–341.
Abiotic stress and control of grain number in cereals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFaru7vN&md5=a2cf44ffe0a8ae493c91c5774254ac66CAS |

Duvick DN (1990) Genetic enhancement and plant breeding. In ‘Advances in new crops’. (Eds J Janick, JE Simon) pp. 90–96. (Timber Press: Portland, OR)

Ellis MH, Rebetzke GJ, Azanza F, Richards RA, Spielmeyer W (2005) Molecular mapping of gibberellin-responsive dwarfing genes in bread wheat. Theoretical and Applied Genetics 111, 423–430.
Molecular mapping of gibberellin-responsive dwarfing genes in bread wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovVKktLc%3D&md5=451830871d3ac35e1e489e6c5b70fd46CAS |

Finch-Savage WE (2004) The use of population-based threshold models to describe and predict the effects of seedbed environment on germination and seedling emergence of crops. In ‘Handbook of seed physiology. Applications to agriculture’. (Eds R Benech-Arnold, RA Sanchez) pp. 51–95. (Food Products Press: New York)

Finch-Savage WE, Clay HA, Lynn JR, Morris K (2010) Towards a genetic understanding of seed vigour in small-seeded crops using natural variation in Brassica oleracea. Plant Science 179, 582–589.
Towards a genetic understanding of seed vigour in small-seeded crops using natural variation in Brassica oleracea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKht7jI&md5=f23402b41d37234510791df2a29b61abCAS |

Fischer RA (1979) Growth and water limitation to dryland wheat yield in Australia: a physiological framework. Journal of the Australian Institute of Agricultural Science 45, 83–94.

Fischer RA, Edmeades GO (2010) Breeding and cereal yield progress. Crop Science 50, S85–S98.
Breeding and cereal yield progress.Crossref | GoogleScholarGoogle Scholar |

Fleury D, Jefferies S, Kuchel H, Langridge P (2010) Genetic and genomic tools to improve drought tolerance in wheat. Journal of Experimental Botany 61, 3211–3222.
Genetic and genomic tools to improve drought tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptVymsLc%3D&md5=126f09449ddbdce476bdc710eb064aceCAS |

Frederiks TM, Christopher JT, Fletcher SEH, Borrell AK (2011) Post head-emergence frost resistance of barley genotypes in the northern grain region of Australia. Crop and Pasture Science 62, 736–745.
Post head-emergence frost resistance of barley genotypes in the northern grain region of Australia.Crossref | GoogleScholarGoogle Scholar |

Furbank RT, Tester M (2011) Phenomics – technologies to relieve the phenotyping bottleneck. Trends in Plant Science 16, 635–644.
Phenomics – technologies to relieve the phenotyping bottleneck.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFOhu7%2FJ&md5=59208026cca4aa61f90a1b57818115edCAS |

Goddard M (2009) Genomic selection: prediction of accuracy and maximisation of long term response. Genetica 136, 245–257.
Genomic selection: prediction of accuracy and maximisation of long term response.Crossref | GoogleScholarGoogle Scholar |

Hall AJ, Richards RA (2012) Prognosis for genetic improvement of yield potential and water-limited yield of major grain crops. Field Crops Research
Prognosis for genetic improvement of yield potential and water-limited yield of major grain crops.Crossref | GoogleScholarGoogle Scholar |

Hammer GL, Chapman S, Van Oosterom E, Podlich DW (2005) Trait physiology and crop modelling as a framework to link phenotypic complexity to underlying genetic systems. Australian Journal of Agricultural Research 56, 947–960.
Trait physiology and crop modelling as a framework to link phenotypic complexity to underlying genetic systems.Crossref | GoogleScholarGoogle Scholar |

Hammer GL, Dong Z, McLean G, Doherty A, Messina C, Schusler J, Zinselmeier C, Paszkiewicz S, Cooper M (2009) Can changes in canopy and/or root system architecture explain historical maize yield trends in the US corn belt? Crop Science 49, 299–312.
Can changes in canopy and/or root system architecture explain historical maize yield trends in the US corn belt?Crossref | GoogleScholarGoogle Scholar |

Harrison MT, Evans JR, Dove H, Moore AD (2011) Dual-purpose cereals: can the relative influences of management and environment on crop recovery and grain yield be dissected? Crop and Pasture Science 62, 930–946.
Dual-purpose cereals: can the relative influences of management and environment on crop recovery and grain yield be dissected?Crossref | GoogleScholarGoogle Scholar |

Henry A, Gowda VRP, Torres RO, McNally KL, Serraj R (2011) Variation in root system architecture and drought response in rice (Oryza sativa): Phenotyping of the OryzaSNP panel in rainfed lowland fields. Field Crops Research 120, 205–214.
Variation in root system architecture and drought response in rice (Oryza sativa): Phenotyping of the OryzaSNP panel in rainfed lowland fields.Crossref | GoogleScholarGoogle Scholar |

Ji X, Shiran B, Wan J, Lewis DC, Jenkins CLD, Condon AG, Richards RA, Dolferus R (2010) Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant, Cell & Environment 33, 926–942.
Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVagsb4%3D&md5=0bde21dd472066df476747943a563387CAS |

Johannsen W (1911) The genotype conception of heredity. American Naturalist 45, 129–159.
The genotype conception of heredity.Crossref | GoogleScholarGoogle Scholar |

Jordan WR (1983) Whole plant response to water deficits: an overview. In ‘Limitations to efficient water use in crop production’. (Eds HM Taylor, WR Jordan, TR Sinclair) pp. 289–317. (American Society of Agronomy: Madison, WI)

Jordan DR, Hunt CH, Cruickshank AW, Borrell AK, Henzell RG (2012) The relationship between the stay-green trait and grain yield in elite sorghum hybrids grown in a range of environments. Crop Science 52, 1153–1161.
The relationship between the stay-green trait and grain yield in elite sorghum hybrids grown in a range of environments.Crossref | GoogleScholarGoogle Scholar |

Kirkegaard JA, Lilley JM, Howe GN, Graham JM (2007) Impact of subsoil water use on wheat yield. Australian Journal of Agricultural Research 58, 303–315.
Impact of subsoil water use on wheat yield.Crossref | GoogleScholarGoogle Scholar |

Lilley JM, Kirkegaard JA (2007) Seasonal variation in the value of subsoil water to wheat: simulation studies in southern New South Wales. Australian Journal of Agricultural Research 58, 1115–1128.
Seasonal variation in the value of subsoil water to wheat: simulation studies in southern New South Wales.Crossref | GoogleScholarGoogle Scholar |

Lopes MS, Reynolds MP (2010) Partitioning of assimilates to deeper roots is associated with cooler canopies and increased yield under drought in wheat. Functional Plant Biology 37, 147–156.
Partitioning of assimilates to deeper roots is associated with cooler canopies and increased yield under drought in wheat.Crossref | GoogleScholarGoogle Scholar |

Lopes MS, Reynolds MP (2012) Stay-green in spring wheat can be determined by spectral reflectance measurements (normalized difference vegetation index) independently from phenology. Journal of Experimental Botany 63, 3789–3798.
Stay-green in spring wheat can be determined by spectral reflectance measurements (normalized difference vegetation index) independently from phenology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVSht7jI&md5=1372de90447f414ccb542a9dd3e06fc6CAS |

Masuka B, Araus JL, Das B, Sonder K, Cairns JE (2012) Phenotyping for abiotic stress tolerance in maize. Journal of Integrative Plant Biology 54, 238–249.
Phenotyping for abiotic stress tolerance in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptVahu7g%3D&md5=d1391b831419642690f5f51f8605ed90CAS |

Messina CD, Podlich D, Dong ZS, Samples M, Cooper M (2011) Yield-trait performance landscapes: from theory to application in breeding maize for drought tolerance. Journal of Experimental Botany 62, 855–868.
Yield-trait performance landscapes: from theory to application in breeding maize for drought tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVekurs%3D&md5=1aec7221ba44e7f226632ea0247894dbCAS |

Mitchell JH, Chapman SC, Rebetzke GJ, Bonnett DG, Fukai S (2012) Evaluation of a reduced-tillering (tin) gene in wheat lines grown across different production environments. Crop and Pasture Science 63, 128–141.
Evaluation of a reduced-tillering (tin) gene in wheat lines grown across different production environments.Crossref | GoogleScholarGoogle Scholar |

Morgan JM, Condon AG (1986) Water-use, grain-yield, and osmoregulation in wheat. Australian Journal of Plant Physiology 13, 523–532.
Water-use, grain-yield, and osmoregulation in wheat.Crossref | GoogleScholarGoogle Scholar |

Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, Ismagul A, Eliby S, Shirley N, Langridge P, Lopato S (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnology Journal 9, 230–249.
Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvVagtL8%3D&md5=a1161caa1812486567dd83c8aed377cbCAS |

Nagel K, Putz A, Gilmer F, Heinz K, Fischbach A, Pfeifer J, Faget M, Blossfeld S, Ernst M, Dimaki C, Kastenholz B, Kleinert A, Galinski A, Scharr H, Fiorani F, Schurr U (2012) GROWSCREEN-Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons. Functional Plant Biology 39, 891–904.
GROWSCREEN-Rhizo is a novel phenotyping robot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons.Crossref | GoogleScholarGoogle Scholar |

Parent B, Suard B, Serraj R, Tardieu F (2010) Rice leaf growth and water potential are resilient to evaporative demand and soil water deficit once the effects of root system are neutralized. Plant, Cell & Environment 33, 1256–1267.

Parish RW, Phan HA, Iacuone S, Li SF (2012) Tapetal development and abiotic stress: a centre of vulnerability. Functional Plant Biology 39, 553–559.
Tapetal development and abiotic stress: a centre of vulnerability.Crossref | GoogleScholarGoogle Scholar |

Passioura JB (2002) Soil conditions and plant growth. Plant, Cell & Environment 25, 311–318.
Soil conditions and plant growth.Crossref | GoogleScholarGoogle Scholar |

Passioura JB (2006) The perils of pot experiments. Functional Plant Biology 33, 1075–1079.
The perils of pot experiments.Crossref | GoogleScholarGoogle Scholar |

Passioura J (2007) The drought environment: physical, biological and agricultural perspectives. Journal of Experimental Botany 58, 113–117.
The drought environment: physical, biological and agricultural perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlOlt7g%3D&md5=572ea8c73aeea3f238e88a52960ce655CAS |

Passioura JB (2010) Scaling up: the essence of effective agricultural research. Functional Plant Biology 37, 585–591.
Scaling up: the essence of effective agricultural research.Crossref | GoogleScholarGoogle Scholar |

Passioura JB, Angus JF (2010) Improving productivity of crops in water-limited environments. Advances in Agronomy 106, 37–75.
Improving productivity of crops in water-limited environments.Crossref | GoogleScholarGoogle Scholar |

Pereira JF, Zhou GF, Delhaize E, Richardson T, Zhou MX, Ryan PR (2010) Engineering greater aluminium resistance in wheat by over-expressing TaALMT1. Annals of Botany 106, 205–214.
Engineering greater aluminium resistance in wheat by over-expressing TaALMT1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWjsLY%3D&md5=25af3803ae3267ca978ee5924f57dd3cCAS |

Poorter H, Bühler J, van Dusschoten D, Climent J, Postma JA (2012a) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Functional Plant Biology 39, 821–838.
Pot size matters: a meta-analysis of the effects of rooting volume on plant growth.Crossref | GoogleScholarGoogle Scholar |

Poorter P, Fiorani F, Stitt M, Schurr U, Finck A, Gibon Y, Usadel B, Munns R, Atkin OK, Tardieu F, Pons TL (2012b) The art of growing plants for experimental purposes; a practical guide for the plant biologist. Functional Plant Biology 39, 839–850.
The art of growing plants for experimental purposes; a practical guide for the plant biologist.Crossref | GoogleScholarGoogle Scholar |

Rebetzke GJ, Condon AG, Richards RA, Farquhar GD (2003) Gene action for leaf conductance in three wheat crosses. Australian Journal of Agricultural Research 54, 381–387.
Gene action for leaf conductance in three wheat crosses.Crossref | GoogleScholarGoogle Scholar |

Rebetzke GJ, Richards RA, Fettell NA, Long M, Condon AG, Forrester RI, Botwright TL (2007) Genotypic increases in coleoptile length improves stand establishment, vigour and grain yield of deep-sown wheat. Field Crops Research 100, 10–23.
Genotypic increases in coleoptile length improves stand establishment, vigour and grain yield of deep-sown wheat.Crossref | GoogleScholarGoogle Scholar |

Rebetzke GJ, Barrett-Lennard EG, Bennett D, Biddulph B, Chenu K, Deery DM, Mayer J, Moeller C, Rattey AR (2012) A multi-site, managed environment facility (MEF) for targeted trait and germplasm phenotyping. Functional Plant Biology 40,

Reynolds M, Tuberosa R (2008) Translational research impacting on crop productivity in drought-prone environments. Current Opinion in Plant Biology 11, 171–179.
Translational research impacting on crop productivity in drought-prone environments.Crossref | GoogleScholarGoogle Scholar |

Richards RA, Rebetzke GJ, Watt M, Condon AG, Spielmeyer W, Dolferus R (2010) Breeding for improved water productivity in temperate cereals: phenotyping, quantitative trait loci, markers and the selection environment. Functional Plant Biology 37, 85–97.
Breeding for improved water productivity in temperate cereals: phenotyping, quantitative trait loci, markers and the selection environment.Crossref | GoogleScholarGoogle Scholar |

Risk JM, Selter LL, Krattinger SG, Viccars LA, Richardson TM, Buesing G, Herren G, Lagudah ES, Keller B (2012) Functional variability of the Lr34 durable resistance gene in transgenic wheat. Plant Biotechnology Journal 10, 477–487.
Functional variability of the Lr34 durable resistance gene in transgenic wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xot1ygs7c%3D&md5=81da7d08be06ea6c8f1de69d5f4584deCAS |

Saini HS, Westgate ME (1999) Reproductive development in grain crops during drought. Advances in Agronomy 68, 59–96.
Reproductive development in grain crops during drought.Crossref | GoogleScholarGoogle Scholar |

Saint Pierre C, Crossa JL, Bonnett D, Yamaguchi-Shinozaki K, Reynolds MP (2012) Phenotyping transgenic wheat for drought resistance. Journal of Experimental Botany 63, 1799–1808.
Phenotyping transgenic wheat for drought resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjslehsb0%3D&md5=a2b275d4624411b31f6ea4d8f58ea335CAS |

Salekdeh GH, Reynolds M, Bennett J, Boyer J (2009) Conceptual framework for drought phenotyping during molecular breeding. Trends in Plant Science 14, 488–496.
Conceptual framework for drought phenotyping during molecular breeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2lurnK&md5=2d2e2c4934dec914c351cca354f3cdafCAS |

Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Current Opinion in Plant Biology 3, 217–223.

Sinclair TR (2011) Challenges in breeding for yield increase for drought. Trends in Plant Science 16, 289–293.
Challenges in breeding for yield increase for drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVyrs74%3D&md5=f6f5d6a65d4982b0344602bb05ce6086CAS |

Stirzaker RJ, Passioura JB, Wilms Y (1996) Soil structure and plant growth: impact of bulk density and biopores. Plant and Soil 185, 151–162.
Soil structure and plant growth: impact of bulk density and biopores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntl2qsw%3D%3D&md5=d7a78bbef7d40f78b54dae3eea6c5763CAS |

Tardieu F (2012) Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. Journal of Experimental Botany 63, 25–31.
Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yms73L&md5=531e0cfde396079dfb6a25550078f074CAS |

Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2011) Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant and Soil 341, 75–87.
Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt1Wjsrc%3D&md5=ed537da3d0db882430dfb58410fbe98eCAS |

Watt M, Kirkegaard JA, Rebetzke GJ (2005) A wheat genotype developed for rapid leaf growth copes well with the physical and biological constraints of unploughed soil. Functional Plant Biology 32, 695–706.
A wheat genotype developed for rapid leaf growth copes well with the physical and biological constraints of unploughed soil.Crossref | GoogleScholarGoogle Scholar |

White JW, Andrade-Sanchez P, Gore MA, Bronson KF, Coffelt TA, Conley MM, Feldmann KA, French AN, Heun JT, Hunsaker DJ, Jenks MA, Kimball BA, Roth RL, Strand RJ, Thorp KR, Wall GW, Wang G (2012) Field-based phenomics for plant genetics research. Field Crops Research 133, 101–112.
Field-based phenomics for plant genetics research.Crossref | GoogleScholarGoogle Scholar |