Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE (Open Access)

Genotypic variation in soil water use and root distribution and their implications for drought tolerance in chickpea

Ramamoorthy Purushothaman A B , Lakshmanan Krishnamurthy A F , Hari D. Upadhyaya A C D , Vincent Vadez A and Rajeev K. Varshney A E
+ Author Affiliations
- Author Affiliations

A International Crops Research Institute for the Semiarid Tropics (ICRISAT), Patancheru 502 324, Telangana, India.

B Jawaharlal Nehru Technological University Hyderabad (JNTUH), Hyderabad 500 085, Telangana, India.

C Department of Agronomy, Kansas State University, 2004 Throckmorton PSC, 1712 Claflin Road, Manhattan, KS 66506, USA.

D UWA Institute of Agriculture, University of Western Australia, 35 Stirling Highway, Crawley, Perth, WA 6009, Australia.

E School of Plant Biology and Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, Perth, WA 6009, Australia.

F Corresponding author. Email: lkm1949@gmail.com

Functional Plant Biology 44(2) 235-252 https://doi.org/10.1071/FP16154
Submitted: 24 April 2016  Accepted: 16 September 2016   Published: 28 November 2016

Journal Compilation © CSIRO Publishing 2017 Open Access CC BY-NC-ND

Abstract

Chickpeas are often grown under receding soil moisture and suffer ~50% yield losses due to drought stress. The timing of soil water use is considered critical for the efficient use of water under drought and to reduce yield losses. Therefore the root growth and the soil water uptake of 12 chickpea genotypes known for contrasts in drought and rooting response were monitored throughout the growth period both under drought and optimal irrigation. Root distribution reduced in the surface and increased in the deep soil layers below 30 cm in response to drought. Soil water uptake was the maximum at 45–60 cm soil depth under drought whereas it was the maximum at shallower (15–30 and 30–45 cm) soil depths when irrigated. The total water uptake under drought was 1-fold less than optimal irrigation. The amount of water left unused remained the same across watering regimes. All the drought sensitive chickpea genotypes were inferior in root distribution and soil water uptake but the timing of water uptake varied among drought tolerant genotypes. Superiority in water uptake in most stages and the total water use determined the best adaptation. The water use at 15–30 cm soil depth ensured greater uptake from lower depths and the soil water use from 90–120 cm soil was critical for best drought adaptation. Root length density and the soil water uptake across soil depths were closely associated except at the surface or the ultimate soil depths of root presence.

Additional keywords: drought tolerance, field phenotyping, root length density, soil water utilisation.


References

Ahmad F, Gaur P, Croser J (2005) Chickpea (Cicer arietinum L.). In ‘Genetic resources, chromosome engineering and crop improvement – grain legumes’. (Eds R Singh, P Jauhar) pp. 185–214. (CRC Press: Boca Raton, FL, USA)

Ali S, Maher AB, Anwar M, Haqqani AM (2002) Exploitation of genetic variability for grain yield improvement in chickpea. International Journal of Agriculture and Biology 4, 148–149.

Álvarez S, Navarro A, Bañón S, Sánchez-Blanco MJ (2009) Regulated deficit irrigation in potted dianthus plants: effects of severe and moderate water stress on growth and physiological responses. Scientia Horticulturae 122, 579–585.
Regulated deficit irrigation in potted dianthus plants: effects of severe and moderate water stress on growth and physiological responses.Crossref | GoogleScholarGoogle Scholar |

Álvarez S, Navarro A, Nicolás E, Sánchez-Blanco MJ (2011) Transpiration, photosynthetic responses, tissue water relations and dry mass partitioning in Callistemon plants during drought conditions. Scientia Horticulturae 129, 306–312.
Transpiration, photosynthetic responses, tissue water relations and dry mass partitioning in Callistemon plants during drought conditions.Crossref | GoogleScholarGoogle Scholar |

Álvarez S, Gómez-Bellot MJ, Castillo M, Bañón S, Sánchez-Blanco MJ (2012) Osmotic and saline effect on growth, water relations, and ion uptake and translocation in Phlomis purpurea plants. Environmental and Experimental Botany 78, 138–145.
Osmotic and saline effect on growth, water relations, and ion uptake and translocation in Phlomis purpurea plants.Crossref | GoogleScholarGoogle Scholar |

Bandyopadhyay PK (2014) Root distribution pattern of pulses in response to water availability. In ‘Resource conservation technology in pulses’. (Eds PK Ghosh, N Kumar, MS Venkatesh, KK Hazra, N Nadarajan) pp. 483–493. (Scientific Publishers: Jodhpur, India)

Bano A, Dorffling K, Bettin D, Hahn H (1993) Abscisic acid and cytokinins as possible root-to-shoot signals in xylem sap of rice plants in drying soil. Australian Journal of Plant Physiology 20, 109–115.
Abscisic acid and cytokinins as possible root-to-shoot signals in xylem sap of rice plants in drying soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXisFWmt7Y%3D&md5=5c2868ffe4ed9398153b641484b25b6eCAS |

Bañon S, Ochoa JF, Sánchez-Blanco MJ, Alarcon JJ (2003) Influence of water deficit and low air humidity in the nursery on survival of Rhamnus alaternus seedlings following planting. Journal of Horticultural Science & Biotechnology 78, 518–522.
Influence of water deficit and low air humidity in the nursery on survival of Rhamnus alaternus seedlings following planting.Crossref | GoogleScholarGoogle Scholar |

Bantilan MCS, Kumara Charyulu D, Gaur PM, Shyam Moses D, Davis J (2014) Short duration chickpea technology: enabling legumes revolution in Andhra Pradesh, India. Research report no. 23. ICRISAT Research Program Markets, Institutions and Policies. ICRISAT, Patancheru, India.

Beebe ST, Rao IM, Blair MW, Butare LO (2009) Breeding for abiotic stress tolerance in common bean: present and future challenges. SABRAO Journal of Breeding and Genetics 41, 1–11.

Benjamin JG, Nielsen DC (2006) Water deficit effects on root distribution of soybean, field pea and chickpea. Field Crops Research 97, 248–253.
Water deficit effects on root distribution of soybean, field pea and chickpea.Crossref | GoogleScholarGoogle Scholar |

Berger JD, Milroy SP, Turner NC, Siddique KHM, Imtiaz M, Malhotra R (2011) Chickpea evolution has selected for contrasting phenological mechanisms among different habitats. Euphytica 180, 1–15.
Chickpea evolution has selected for contrasting phenological mechanisms among different habitats.Crossref | GoogleScholarGoogle Scholar |

Bernier J, Serraj R, Kumar A, Venuprasad R, Impa S, Gowda V, Oane R, Spaner D, Atlin G (2009) Increased water uptake explains the effect of qtl12.1, a large-effect drought-resistance QTL in upland rice. Field Crops Research 110, 139–146.
Increased water uptake explains the effect of qtl12.1, a large-effect drought-resistance QTL in upland rice.Crossref | GoogleScholarGoogle Scholar |

Bishopp A, Lynch JP (2015) The hidden half of crop yields. Nature Plants 1, 15117
The hidden half of crop yields.Crossref | GoogleScholarGoogle Scholar |

Blum A (2009) Effective use of water (EUW) and not water-use efficiency is the target of crop yield improvement under drought stress. Field Crops Research 112, 119–123.
Effective use of water (EUW) and not water-use efficiency is the target of crop yield improvement under drought stress.Crossref | GoogleScholarGoogle Scholar |

Borrell AK, Mullet JE, George-Jaeggli B, van Oosterom EJ, Hammer GL, Klein PE, Jordan DR (2014) Drought adaptation of stay-green sorghum is associated with canopy development, leaf anatomy, root growth, and water uptake. Journal of Experimental Botany 65, 6251–6263.
Drought adaptation of stay-green sorghum is associated with canopy development, leaf anatomy, root growth, and water uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitl2gsbc%3D&md5=f0fb956421f7cf7433ed636792d481abCAS |

Chauhan YS, Nene YL, Johansen C, Haware MP, Saxena NP, Singh S, Sharma SB, Sahrawat KL, Burford JR, Rupela OP, Kumar Rao JVDK, Sithanantham S (1988) Effects of soil solarization on pigeonpea and chickpea. Research bulletin no. 11. ICRISAT, Patancheru, India.

Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought: from genes to the whole plant. Functional Plant Biology 30, 239–264.
Understanding plant responses to drought: from genes to the whole plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVKlt7o%3D&md5=0c43359463e985e3294c3b6104992db2CAS |

Chimungu JG, Brown KM, Lynch JP (2014a) Large root cortical cell size improves drought tolerance in maize (Zea mays L.). Plant Physiology 166, 2166–2178.
Large root cortical cell size improves drought tolerance in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |

Chimungu JG, Brown KM, Lynch JP (2014b) Reduced root cortical cell file number improves drought tolerance in maize. Plant Physiology 166, 1943–1955.
Reduced root cortical cell file number improves drought tolerance in maize.Crossref | GoogleScholarGoogle Scholar |

Chyliński WK, Łukaszewska AJ, Kutnik K (2007) Drought response of two bedding plants. Acta Physiologiae Plantarum 29, 399–406.
Drought response of two bedding plants.Crossref | GoogleScholarGoogle Scholar |

CIAT (2007) Annual report. Outcome line SBA-1. Improved beans for the developing world: 120. ICRISAT, Patancheru, India.

CIAT (2008) Annual report. Outcome line SBA-1. Improved beans for the developing world: 39–65. ICRISAT, Patancheru, India.

Comas LH, Anderson LJ, Dunst RM, Lakso AN, Eissenstat DM (2005) Canopy and environmental control of root dynamics in a long-term study of Concord grape. New Phytologist 167, 829–840.
Canopy and environmental control of root dynamics in a long-term study of Concord grape.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2Mvjs1Ohtg%3D%3D&md5=bb84a26da54e17ea356ccf1eef751476CAS |

Comas LH, Becker SR, Cruz VM, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Frontiers in Plant Science 4, 442
Root traits contributing to plant productivity under drought.Crossref | GoogleScholarGoogle Scholar |

Cutforth HW, Angadi SV, McConkey BG, Miller PR, Ulrich D, Gulden R, Volkmar KM, Entz MH, Brandt SA (2013) Comparing rooting characteristics and soil water withdrawal patterns of wheat with alternative oilseed and pulse crops grown in the semiarid Canadian prairie. Canadian Journal of Soil Science 93, 147–160.
Comparing rooting characteristics and soil water withdrawal patterns of wheat with alternative oilseed and pulse crops grown in the semiarid Canadian prairie.Crossref | GoogleScholarGoogle Scholar |

Dardanelli JL, Ritchie JT, Calmon M, Andriani JM, Collino DJ (2004) An empirical model for root water uptake. Field Crops Research 87, 59–71.
An empirical model for root water uptake.Crossref | GoogleScholarGoogle Scholar |

Davies FT, Olade-Portugal V, Aguilera-Gomez L, Alvarado MJ, Ferrera-Cerrato RC, Boutton TW (2002) Alleviation of drought stress of Chile ancho pepper (Capsicum annuum L. cv. San Luis) with arbuscular mycorrhiza indigenous to Mexico. Scientia Horticulturae 92, 347–359.
Alleviation of drought stress of Chile ancho pepper (Capsicum annuum L. cv. San Luis) with arbuscular mycorrhiza indigenous to Mexico.Crossref | GoogleScholarGoogle Scholar |

De Sousa MA, Lima MDB (2010) Influence of suppression of the irrigation in stages of growth of bean cv. Carioca comum. Bioscience Journal 26, 550–557.

dos Santos TP, Lopes CM, Rodrigues ML, Souza CR, Silva JR, Maroco JP, Pereira JS, Chaves MM (2007) Effects of deficit irrigation strategies on cluster microclimate for improving fruit composition of Moscatel field-grown grapevines. Scientia Horticulturae 112, 321–330.
Effects of deficit irrigation strategies on cluster microclimate for improving fruit composition of Moscatel field-grown grapevines.Crossref | GoogleScholarGoogle Scholar |

Drew MC, Webb J, Saker LR (1990) Regulation of K+ uptake and transport to the xylem in barley roots; K+ distribution determined by electron probe X-ray microanalysis of frozen-hydrated cells. Journal of Experimental Botany 41, 815–825.
Regulation of K+ uptake and transport to the xylem in barley roots; K+ distribution determined by electron probe X-ray microanalysis of frozen-hydrated cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXjvFanug%3D%3D&md5=49ed05eb64c0ef736575e2cfffea069fCAS |

Eghball B, Maranville JW (1993) Root development and nitrogen influx of corn genotypes grown under combined drought and nitrogen stresses. Agronomy Journal 85, 147–152.
Root development and nitrogen influx of corn genotypes grown under combined drought and nitrogen stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitFWqtL8%3D&md5=521e8955b511b886d171c6c1784e3c6fCAS |

El-Swaify SA, Pathak P, Rego TJ, Singh S (1985) Soil management for optimized productivity under rainfed conditions in the semi-arid tropics. In ‘Advances in soil science.’ pp. 1–64. (Springer-Verlag: New York)

Evans LT (1998) ‘Feeding the ten billion: plants and population growth.’ (Cambridge University Press: Cambridge, UK)

FAOSTAT (2014) ‘FAO statistics division.’ Available at http://faostat3.fao.org/compare/E [Verified 27 February 2016].

Fenta BA, Beebe SE, Kunert KJ, Burridge JD, Barlow KM, Lynch JP, Foyer CH (2014) Field phenotyping of soybean roots for drought stress tolerance. Agronomy 4, 418–435.
Field phenotyping of soybean roots for drought stress tolerance.Crossref | GoogleScholarGoogle Scholar |

Fischer RA, Rees D, Sayre KD, Lu ZM, Condon AG, Saavedra AL (1998) Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Crop Science 38, 1467–1475.
Wheat yield progress associated with higher stomatal conductance and photosynthetic rate, and cooler canopies.Crossref | GoogleScholarGoogle Scholar |

Franco JA, Arreola J, Vicente MJ, Martinez-Sanchez JJ (2008) Nursery irrigation regimes affect the seedling characteristics of Silene vulgaris as they relate to potential performance following transplanting into semi-arid conditions. Journal of Horticultural Science & Biotechnology 83, 15–22.
Nursery irrigation regimes affect the seedling characteristics of Silene vulgaris as they relate to potential performance following transplanting into semi-arid conditions.Crossref | GoogleScholarGoogle Scholar |

Franco JA, Bañón S, Vicente MJ, Miralles J, Martínez-Sánchez JJ (2011) Root development in horticultural plants grown under abiotic stress conditions – a review. Journal of Horticultural Science & Biotechnology 86, 543–556.
Root development in horticultural plants grown under abiotic stress conditions – a review.Crossref | GoogleScholarGoogle Scholar |

Gaur PM, Jukanti AK, Samineni S, Chaturvedi SK, Basu PS, Babbar A, Jayalakshmi V, Nayyar H, Devasirvatham V, Mallikarjuna N, Krishnamurthy L (2014) Climate change and heat stress tolerance in chickpea. In ‘Climate change and plant abiotic stress tolerance’. (Eds N Tuteja, SS Gill) pp. 837 –856. (Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, Germany)

Gowda CLL, Singh O, Sethi SC, Singh KB, Rao BV, Rahman MM, Kumar J, Rahman MA (1995) Registration of ‘ICCV 10’ chickpea. Crop Science 35, 589
Registration of ‘ICCV 10’ chickpea.Crossref | GoogleScholarGoogle Scholar |

Gowda VR, Henry A, Vadez V, Shashidhar HE, Serraj R (2012) Water uptake dynamics under progressive drought stress in diverse accessions of the OryzaSNP panel of rice (Oryza sativa). Functional Plant Biology 39, 402–411.
Water uptake dynamics under progressive drought stress in diverse accessions of the OryzaSNP panel of rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar |

Gregory PJ (1994) Resource capture by root networks. In ‘Resource capture by crops’. (Eds JL Monteith, RK Scott, MH Unsworth) pp. 77–97. (Nottingham University Press: Nottingham, UK)

Guswa AJ (2008) The influence of climate on root depth: a carbon cost‐benefit analysis. Water Resources Research 1, 44

Hammer GL, Dong Z, McLean G, Doherty A, Messina C, Schussler 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 |

Hammer GL, van Oosterom E, McLean G, Chapman SC, Broad I, Harland P, Muchow RC (2010) Adapting APSIM to model the physiology and genetics of complex adaptive traits in field crops. Journal of Experimental Botany 61, 2185–2202.
Adapting APSIM to model the physiology and genetics of complex adaptive traits in field crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsVGnsr0%3D&md5=90c0f43966d4bb18e2740adb745f5548CAS |

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 |

ICRISAT (1992) ‘ICC 4958 A drought resistant chickpea. Plant material description no. 33.’ (ICRISAT: Patancheru, India)

Itoh H, Hayashi S, Nakajima T, Hayashi T, Yoshida H, Yamazaki K, Komatsu T (2009) Effects of soil type, vertical root distribution and precipitation on grain yield of winter wheat. Plant Production Science 12, 503–513.
Effects of soil type, vertical root distribution and precipitation on grain yield of winter wheat.Crossref | GoogleScholarGoogle Scholar |

Jaramillo RE, Nord EA, Chimungu JG, Brown KM, Lynch JP (2013) Root cortical burden influences drought tolerance in maize. Annals of Botany 112, 429–437.
Root cortical burden influences drought tolerance in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSitbbK&md5=edfd402ae015084bfc1393663a040a69CAS |

Johansen C, Singh DN, Krishnamurthy L, Saxena NP, Chauhan YS, Kumar Rao JVDK (1997) Options for alleviating moisture stress in pulse crops. In ‘Recent advances in pulses research’. (Eds AN Asthana, A Masood) pp. 425–442. (Indian Society of Pulses Research and Development: Kanpur, India)

Jones JW, Zur B (1984) Simulation of possible adaptive mechanisms in crops subjected to water stress. Irrigation Science 5, 251–264.
Simulation of possible adaptive mechanisms in crops subjected to water stress.Crossref | GoogleScholarGoogle Scholar |

Jordan WR, Dugas WA, Shouse PJ (1983) Strategies for crop improvement drought-prone region (Sorghum bicolor, Triticum aestivum, wheat plant breeding). Agricultural Water Management 7, 281–299.
Strategies for crop improvement drought-prone region (Sorghum bicolor, Triticum aestivum, wheat plant breeding).Crossref | GoogleScholarGoogle Scholar |

Kamoshita A, Wade L, Yamauchi A (2000) Genotypic variation in response of rainfed lowland rice to drought and rewatering: 3. Water extraction during the drought period. Plant Production Science 3, 189–196.
Genotypic variation in response of rainfed lowland rice to drought and rewatering: 3. Water extraction during the drought period.Crossref | GoogleScholarGoogle Scholar |

Kanwar JS, Kampen J, Virmani SM (1982) ‘Management of Vertisols for maximising crop production-ICRISAT experience.’ In ‘Vertisols and rice soils of the tropics. Transacctions of the 12th international congress of soil science. Vol. 3’. pp. 94–118. (Indian Society of Soil Science: New Delhi)

Kashiwagi J, Krishnamurthy L, Upadhyaya HD, Krishna H, Chandra S, Vadez V, Serraj R (2005) Genetic variability of drought-avoidance root traits in the mini-core germplasm collection of chickpea (Cicer arietinum L.). Euphytica 146, 213–222.

Kashiwagi J, Krishnamurthy L, Crouch JH, Serraj R (2006) Variability of root length density and its contributions to seed yield in chickpea (Cicer arietinum L.) under terminal drought stress. Field Crops Research 95, 171–181.
Variability of root length density and its contributions to seed yield in chickpea (Cicer arietinum L.) under terminal drought stress.Crossref | GoogleScholarGoogle Scholar |

Kashiwagi J, Krishnamurthy L, Upadhyaya HD, Gaur PM (2008) Rapid screening technique for canopy temperature status and its relevance to drought tolerance improvement in chickpea. Journal of SAT Agricultural Research 6, 1–4.

Kashiwagi J, Krishnamurthy L, Gaur PM, Upadhyaya HD, Varshney RK, Tobita S (2013) Traits of relevance to improve yield under terminal drought stress in chickpea (C. arietinum L.). Field Crops Research 145, 88–95.
Traits of relevance to improve yield under terminal drought stress in chickpea (C. arietinum L.).Crossref | GoogleScholarGoogle Scholar |

Kashiwagi J, Krishnamurthy L, Purushothaman R, Upadhyaya HD, Gaur PM, Gowda CLL, Ito O, Varshney RK (2015) Scope for improvement of yield under drought through the root traits in chickpea (Cicer arietinum L.). Field Crops Research 170, 47–54.
Scope for improvement of yield under drought through the root traits in chickpea (Cicer arietinum L.).Crossref | GoogleScholarGoogle Scholar |

Kell DB (2011) Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water sequestration. Annals of Botany 108, 407–418.
Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water sequestration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVygsLjM&md5=04b690547d43406d5e43a0f3b88189a0CAS |

Koike T, Kitao M, Quoreshi AM, Matsuura Y (2003) Growth characteristics of root–shoot relations of three birch seedlings raised under different water regimes. Plant and Soil 255, 303–310.
Growth characteristics of root–shoot relations of three birch seedlings raised under different water regimes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotV2js7Y%3D&md5=d4afc6a3bc49d5c3ee85c1ecd17c22c5CAS |

Konings H, Jackson MB (1979) A relationship between rates of ethylene production by roots and the promoting or inhibiting effects of exogenous ethylene and water on root elongation. Zeitschrift für Pflanzenphysiologie 92, 385–397.
A relationship between rates of ethylene production by roots and the promoting or inhibiting effects of exogenous ethylene and water on root elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXktFGit7w%3D&md5=ff24b4ecb27110715b72dcf353f93312CAS |

Kramer PJ, Boyer JS (1995) ‘Water relations of plants and soils.’ (Academic Press: San Diego, CA, USA)

Krishnamurthy L, Johansen C, Sethi SC (1999) Investigation of factors determining genotypic differences in seed yield of non-irrigated and irrigated chickpeas using a physiological model of yield determination. Journal Agronomy & Crop Science 183, 9–17.
Investigation of factors determining genotypic differences in seed yield of non-irrigated and irrigated chickpeas using a physiological model of yield determination.Crossref | GoogleScholarGoogle Scholar |

Krishnamurthy L, Kashiwagi J, Gaur PM, Upadhyaya HD, Vadez V (2010) Sources of tolerance to terminal drought in the chickpea (Cicer arietinum L.) minicore germplasm. Field Crops Research 119, 322–330.
Sources of tolerance to terminal drought in the chickpea (Cicer arietinum L.) minicore germplasm.Crossref | GoogleScholarGoogle Scholar |

Krishnamurthy L, Kashiwagi J, Upadhyaya HD, Gowda CLL, Gaur PM, Singh S, Purushothaman R, Varshney RK (2013) Partitioning coefficient – a trait that contributes to drought tolerance in chickpea. Field Crops Research 149, 354–365.
Partitioning coefficient – a trait that contributes to drought tolerance in chickpea.Crossref | GoogleScholarGoogle Scholar |

Kulkarni M, Deshpande U (2007) Gradient in vitro testing of tomato (Solanum lycopersicon L.) cultivars by inducing water deficit – a new approach to screen germplasm for drought tolerance. Asian Journal of Plant Science 6, 934–940.
Gradient in vitro testing of tomato (Solanum lycopersicon L.) cultivars by inducing water deficit – a new approach to screen germplasm for drought tolerance.Crossref | GoogleScholarGoogle Scholar |

Kumar J, Abbo S (2001) Genetics of flowering time in chickpea and its bearing on productivity in semiarid environments. Advances in Agronomy 2, 122

Kumar J, Rao BV (2001) Registration of ICCV 96029, super early and double podded chickpea germplasm. Crop Science 41, 605–606.
Registration of ICCV 96029, super early and double podded chickpea germplasm.Crossref | GoogleScholarGoogle Scholar |

Kumar J, Haware MP, Smithon JB (1985) Registration of four short-duration Fusarium wilt-resistant kabuli (Garbanzo) chickpea germplasm. Crop Science 25, 576–577.
Registration of four short-duration Fusarium wilt-resistant kabuli (Garbanzo) chickpea germplasm.Crossref | GoogleScholarGoogle Scholar |

Kumar B, Abdel‐Ghani AH, Reyes‐Matamoros J, Hochholdinger F, Lübberstedt T (2012) Genotypic variation for root architecture traits in seedlings of maize (Zea mays L.) inbred lines. Plant Breeding 131, 465–478.
Genotypic variation for root architecture traits in seedlings of maize (Zea mays L.) inbred lines.Crossref | GoogleScholarGoogle Scholar |

Lafitte HR, Champoux MC, McLaren G, O’Toole JC (2001) Rice root morphological traits are related to isozyme group and adaptation. Field Crops Research 71, 57–70.
Rice root morphological traits are related to isozyme group and adaptation.Crossref | GoogleScholarGoogle Scholar |

Lambers H, Atkin OK, Millenaar FF (2002) Respiratory patterns in roots in relation to their functioning. In ‘Plant roots: the hidden half’. (Eds Y Waisel, A Eshel, K Kafkaki) pp. 521–552. (Marcel Dekker Inc.: New York)

Liao MT, Fillery IRP, Palta JA (2004) Early vigorous growth is a major factor influencing nitrogen uptake in wheat. Functional Plant Biology 31, 121–129.
Early vigorous growth is a major factor influencing nitrogen uptake in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsl2gtrk%3D&md5=132d4a2fb4c0b031026c7444b6a80fa9CAS |

Liu L, Gan Y, Bueckert R, Van Rees K (2011) Rooting systems of oilseed and pulse crops. II: Vertical distribution patterns across the soil profile. Field Crops Research 122, 248
Rooting systems of oilseed and pulse crops. II: Vertical distribution patterns across the soil profile.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 |

Ludlow MM, Muchow RC (1990) A critical evaluation of traits for improving crop yields in water-limited environments. Advances in Agronomy 43, 107–153.
A critical evaluation of traits for improving crop yields in water-limited environments.Crossref | GoogleScholarGoogle Scholar |

Lush JL (1940) Intra-sire correlation and regression of offspring on dams as a method of estimating heritability of characters. Proceedings of the American Society of Animal Nutrition 33, 293–301.

Lynch JP (1995) Root architecture and plant productivity. Plant Physiology 109, 7–13.

Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Annals of Botany 112, 347–357.
Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSitbfJ&md5=03958de958e36d07f3233d52724a7053CAS |

Lynch JP, Chimungu JG, Brown KM (2014) Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement. Journal of Experimental Botany 65, 6155–6166.
Root anatomical phenes associated with water acquisition from drying soil: targets for crop improvement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitl2gsbw%3D&md5=74ab7a97947fb65dcaa8aa44071691caCAS |

Ma SC, Li FM, Xu BC, Huang ZB (2010) Effect of lowering the root/shoot ratio by pruning roots on water use efficiency and grain yield of winter wheat. Field Crops Research 115, 158–164.
Effect of lowering the root/shoot ratio by pruning roots on water use efficiency and grain yield of winter wheat.Crossref | GoogleScholarGoogle Scholar |

Manavalan LP, Musket T, Nguyen HT (2011) Natural genetic variation for root traits among diversity lines of maize (Zea mays L.). Maydica 56, 1707

Manschadi AM, Christopher JT, Hammer GL, deVoil P (2010) Experimental and modelling studies of drought‐adaptive root architectural traits in wheat (Triticum aestivum L.). Plant Biosystems 144, 458–462.
Experimental and modelling studies of drought‐adaptive root architectural traits in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |

Mishra HS, Rathore TR, Savita US (2001) Water use efficiency of irrigated winter maize under cool weather conditions of India. Irrigation Science 21, 27–33.
Water use efficiency of irrigated winter maize under cool weather conditions of India.Crossref | GoogleScholarGoogle Scholar |

Molz FJ, Remson I (1970) Extraction term models of soil moisture use by transpiring plants. Water Resources Research 6, 1346–1356.
Extraction term models of soil moisture use by transpiring plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXjtFWiug%3D%3D&md5=6748e99c6d53b78374838e344c66b8f7CAS |

Moroke TS, Schwartz RC, Brown KW, Juo ASR (2005) Soil water depletion and root distribution of three dryland crops. Soil Science Society of America Journal 69, 197–205.
Soil water depletion and root distribution of three dryland crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnvFGltA%3D%3D&md5=8832c2688830b0ed6807ec99f55fd17bCAS |

Navarro A, Álvarez S, Castillo M, Bañón S, Sánchez-Blanco MJ (2009) Changes in tissue-water relations, photosynthetic activity, and growth of Myrtus communis plants in response to different conditions of water availability. Journal of Horticultural Science & Biotechnology 84, 541
Changes in tissue-water relations, photosynthetic activity, and growth of Myrtus communis plants in response to different conditions of water availability.Crossref | GoogleScholarGoogle Scholar |

Nord EA, Lynch JP (2009) Plant phenology: a critical controller of soil resource acquisition. Journal of Experimental Botany 60, 1927–1937.
Plant phenology: a critical controller of soil resource acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFSjur8%3D&md5=8b9860ad01c9c8f75d65bc3cf3ae923bCAS |

Okada K, Kondo M, Ando H, Kakuda K (2002) Water uptake under water stress at panicle initiation stage in upland rice as affected by previous soil water regimes. Soil Science and Plant Nutrition 48, 151–158.
Water uptake under water stress at panicle initiation stage in upland rice as affected by previous soil water regimes.Crossref | GoogleScholarGoogle Scholar |

Pandey RK, Maranville JW, Admou A (2000a) Deficit irrigation and nitrogen effects on maize in a Sahelian environment: I. Grain yield and yield components. Agricultural Water Management 46, 1–13.
Deficit irrigation and nitrogen effects on maize in a Sahelian environment: I. Grain yield and yield components.Crossref | GoogleScholarGoogle Scholar |

Pandey RK, Maranville JW, Chetima MM (2000b) Deficit irrigation and nitrogen effects on maize in a Sahelian environment: II. Shoot growth, nitrogen uptake and water extraction. Agricultural Water Management 46, 15–27.
Deficit irrigation and nitrogen effects on maize in a Sahelian environment: II. Shoot growth, nitrogen uptake and water extraction.Crossref | GoogleScholarGoogle Scholar |

Pinheiro HA, DaMatta FM, Chaves ARM, Loureiro ME, Ducatti C (2005) Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora. Annals of Botany 96, 101–108.
Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora.Crossref | GoogleScholarGoogle Scholar |

Puangbut D, Jogloy S, Vorasoot N, Akkasaeng C, Kesmala T, Rachaputi RCN, Wright GC, Patanothai A (2009) Association of root dry weight and transpiration efficiency of peanut genotypes under early season drought. Agricultural Water Management 96, 1460–1466.
Association of root dry weight and transpiration efficiency of peanut genotypes under early season drought.Crossref | GoogleScholarGoogle Scholar |

Purushothaman R, Upadhyaya HD, Gaur PM, Gowda CLL, Krishnamurthy L (2014) Kabuli and desi chickpeas differ in their requirement for reproductive duration. Field Crops Research 163, 24–31.
Kabuli and desi chickpeas differ in their requirement for reproductive duration.Crossref | GoogleScholarGoogle Scholar |

Purushothaman R, Thudi M, Krishnamurthy L, Upadhyaya HD, Kashiwagi J, Gowda CLL, Varshney RK (2015) Association of mid-reproductive stage canopy temperature depression with the molecular markers and grain yields of chickpea (Cicer arietinum L.) germplasm under terminal drought. Field Crops Research 174, 1–11.
Association of mid-reproductive stage canopy temperature depression with the molecular markers and grain yields of chickpea (Cicer arietinum L.) germplasm under terminal drought.Crossref | GoogleScholarGoogle Scholar |

Purushothaman R, Krishnamurthy L, Upadhyaya HD, Vadez V, Varshney RK (2016) Shoot traits and their relevance in terminal drought tolerance of chickpea (Cicer arietinum L.). Field Crops Research 197, 10–27.

Ratnakumar P, Vadez V, Nigam SN, Krishnamurthy L (2009) Assessment of transpiration efficiency in peanut (Arachis hypogaea L.) under drought using a lysimetric system. Plant Biology 11, 124–130.
Assessment of transpiration efficiency in peanut (Arachis hypogaea L.) under drought using a lysimetric system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslajsrc%3D&md5=98e96a8bb795f4561c4883aa81982344CAS |

Richards RA, Passioura JB (1989) A breeding program to reduce the diameter of the major xylem vessel in the seminal roots of wheat and its effect on grain yield in rain-fed environments. Australian Journal of Agricultural Research 40, 943–950.
A breeding program to reduce the diameter of the major xylem vessel in the seminal roots of wheat and its effect on grain yield in rain-fed environments.Crossref | GoogleScholarGoogle Scholar |

Ritchie JT (1981) Soil water availability. Plant and Soil 58, 327–338.
Soil water availability.Crossref | GoogleScholarGoogle Scholar |

Robertson WK, Hammond LC, Johnson JT, Boote KJ (1980) Effects of plant-water stress on root distribution of corn, soybeans, and peanuts in sandy soil. Agronomy Journal 72, 548–550.
Effects of plant-water stress on root distribution of corn, soybeans, and peanuts in sandy soil.Crossref | GoogleScholarGoogle Scholar |

Ryan JG (1997) A global perspective on pigeonpea and chickpea sustainable production systems: present status and future potential. In ‘Recent advances in pulses research’. (Eds AN Asthana, M Ali) pp. 1–31. (Indian Society of Pulses Research and Development: Kanpur, India)

Sabaghpour SH, Kumar J, Rao TN (2003) Inheritance of growth vigour and its association with other characters in chickpea. Plant Breeding 122, 542–544.
Inheritance of growth vigour and its association with other characters in chickpea.Crossref | GoogleScholarGoogle Scholar |

Sánchez-Blanco MJ, Rodríguez P, Morales MA, Ortuño MF, Torrecillas A (2002) Comparative growth and water relation of Cistus albidus and Cistus monspeliensis plants during water deficit conditions and recovery. Plant Science 162, 107–113.
Comparative growth and water relation of Cistus albidus and Cistus monspeliensis plants during water deficit conditions and recovery.Crossref | GoogleScholarGoogle Scholar |

Sauter A, Davies WJ, Hartung W (2001) The long‐distance abscisic acid signal in the droughted plant: the fate of the hormone on its way from root to shoot. Journal of Experimental Botany 52, 1991–1997.
The long‐distance abscisic acid signal in the droughted plant: the fate of the hormone on its way from root to shoot.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXns1Wkt78%3D&md5=c698b4b143d441e4d2bda0fdaa2900acCAS |

Saxena NP, Krishnamurthy L, Johansen C (1993) Registration of a drought-resistant chickpea germplasm. Crop Science 33, 1424
Registration of a drought-resistant chickpea germplasm.Crossref | GoogleScholarGoogle Scholar |

Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annual Review of Plant Biology 58, 47–69.
Nutrient sensing and signaling: NPKS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsVahs74%3D&md5=6a0bf403a79acf4fc1ca111869ce59a1CAS |

Schoppach RM, Wauthelet D, Jeanguenin L, Sadok W (2014) Conservative water use under high evaporative demand associated with smaller root metaxylem and limited trans-membrane water transport in wheat. Functional Plant Biology 41, 257–269.
Conservative water use under high evaporative demand associated with smaller root metaxylem and limited trans-membrane water transport in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisF2rs7s%3D&md5=8a6d2bb792bf56ce5ccc071a9cba0730CAS |

Searle SR (1961) Phenotypic, genetic and environmental correlations. Biometrics 17, 474–480.
Phenotypic, genetic and environmental correlations.Crossref | GoogleScholarGoogle Scholar |

Serraj R, Krishnamurthy L, Kashiwagi J, Kumar J, Chandra S, Crouch JH (2004) Variation in root traits of chickpea (Cicer arietinum L.) grown under terminal drought. Field Crops Research 88, 115–127.
Variation in root traits of chickpea (Cicer arietinum L.) grown under terminal drought.Crossref | GoogleScholarGoogle Scholar |

Sharp RE, Davies WJ (1985) Root growth and water uptake by maize plants in drying soils. Journal of Experimental Botany 36, 1441–1456.
Root growth and water uptake by maize plants in drying soils.Crossref | GoogleScholarGoogle Scholar |

Silim SN, Saxena MC (1993) Adaptation of spring-sown chickpea to the Mediterranean basin: I. Response to moisture supply. Field Crops Research 34, 121–136.
Adaptation of spring-sown chickpea to the Mediterranean basin: I. Response to moisture supply.Crossref | GoogleScholarGoogle Scholar |

Sinclair TR (1994) Limits to crop yield? In ‘Physiology and determination of crop yield’. (Ed. KJ Boote) pp. 509–532. (ASA, CSSA and SSSA: Madison, WI, USA)

Soltani A, Ghassemi-Golezani K, Khooie FR, Moghaddam M (1999) A simple model for chickpea growth and yield. Field Crops Research 62, 213–224.
A simple model for chickpea growth and yield.Crossref | GoogleScholarGoogle Scholar |

Soltani A, Khooie FR, Ghassemi-Golezani K, Moghaddam M (2000) Thresholds for chickpea leaf expansion and transpiration response to soil water deficit. Field Crops Research 68, 205–210.
Thresholds for chickpea leaf expansion and transpiration response to soil water deficit.Crossref | GoogleScholarGoogle Scholar |

Sponchiado BN, White JW, Castillo JA, Jones PG (1980) Root growth of four common bean cultivars in relation to drought tolerance in environments with contrasting soil types. Experimental Agriculture 25, 249–257.
Root growth of four common bean cultivars in relation to drought tolerance in environments with contrasting soil types.Crossref | GoogleScholarGoogle Scholar |

Steele KA, Price AH, Witcombe JR, Shrestha R, Singh BN, Gibbons JM, Virk DS (2013) QTLs associated with root traits increase yield in upland rice when transferred through marker-assisted selection. Theoretical and Applied Genetics 126, 101–108.
QTLs associated with root traits increase yield in upland rice when transferred through marker-assisted selection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bmtFylsQ%3D%3D&md5=057fd07dbd31ca03c3fe41c46cc32063CAS |

Suji KK, Prince KS, Mankhar PS, Kanagaraj P, Poornima R, Amutha K, Kavitha S, Biji KR, Gomez SM, Babu RC (2012) Evaluation of rice (Oryza sativa L.) near iso-genic lines with root QTLs for plant production and root traits in rainfed target populations of environment. Field Crops Research 137, 89–96.
Evaluation of rice (Oryza sativa L.) near iso-genic lines with root QTLs for plant production and root traits in rainfed target populations of environment.Crossref | GoogleScholarGoogle Scholar |

Trachsel S, Stamp P, Hund A (2010) Growth of axile and lateral roots of maize: response to desiccation stress induced by polyethylene glycol 8000. Maydica 55, 101–109.

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=290d705e20e1a515b744831364899db4CAS |

Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genetics 45, 1097–1102.
Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1WgsrnM&md5=e30633885a519fbf67b1d41ca339c4f8CAS |

Vadez V, Soltani A, Sinclair TR (2012) Modelling possible benefits of root related traits to enhance terminal drought adaptation of chickpea. Field Crops Research 137, 108–115.
Modelling possible benefits of root related traits to enhance terminal drought adaptation of chickpea.Crossref | GoogleScholarGoogle Scholar |

Wang X, Gan Y, Hamel C, Lemke R, McDonald C (2012) Water use profiles across the rooting zones of various pulse crops. Field Crops Research 134, 130–137.
Water use profiles across the rooting zones of various pulse crops.Crossref | GoogleScholarGoogle Scholar |

Wasson AP, Richards RA, Chatrath R, Misra SC, Prasad SV, Rebetzke GJ, Kirkegaard JA, Christopher J, Watt M (2012) Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. Journal of Experimental Botany 63, 3485–3498.
Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVSit7c%3D&md5=8ca794a1ea3b5795ff5bc20412c2692dCAS |

Wasson AP, Rebetzke GJ, Kirkegaard JA, Christopher J, Richards RA, Watt M (2014) Soil coring at multiple field environments can directly quantify variation in deep root traits to select wheat genotypes for breeding. Journal of Experimental Botany 65, 6231–6249.
Soil coring at multiple field environments can directly quantify variation in deep root traits to select wheat genotypes for breeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitl2gsbY%3D&md5=dcfb209a8c1835b48a4cea3afa8fac34CAS |

White JW, Castillo JA (1992) Evaluation of diverse shoot genotypes on selected root genotypes of common bean under soil water deficits. Crop Science 32, 762–765.
Evaluation of diverse shoot genotypes on selected root genotypes of common bean under soil water deficits.Crossref | GoogleScholarGoogle Scholar |

Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant, Cell & Environment 25, 195–210.
ABA-based chemical signalling: the co-ordination of responses to stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhslaktbY%3D&md5=2a09a62a6ca64bb64b171adad021cfd9CAS |

Yu GR, Zhuang J, Nakayama K, Jin Y (2007) Root water uptake and profile soil water as affected by vertical root distribution. Plant Ecology 189, 15–30.
Root water uptake and profile soil water as affected by vertical root distribution.Crossref | GoogleScholarGoogle Scholar |

Zaman-Allah M, Jenkinson DM, Vadez V (2011) A conservative pattern of water use, rather than deep or profuse rooting, is critical for the terminal drought tolerance of chickpea. Journal of Experimental Botany 62, 4239–4252.
A conservative pattern of water use, rather than deep or profuse rooting, is critical for the terminal drought tolerance of chickpea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVeit7jJ&md5=92e474048222fd32771055d9f1286ec5CAS |

Zhu J, Brown KM, Lynch JP (2010) Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). Plant, Cell & Environment 33, 740–749.