Is heterosis in maize mediated through better water use?
*Heterosis increases yield potential and improves adaptation to stress in maize (Zea mays); however, the underlying mechanisms remain elusive. *A set of tropical inbred lines and their hybrids were grown in the field for 2 yr under three different water regimes. First-year plant water use was evaluated by measuring instantaneous traits (stomatal conductance (g(s)) and steady-state chlorophyll fluorescence (F(s))) in individual leaves together with time-integrative traits, which included mineral accumulation in the whole leaves of plants and oxygen isotope enrichment above source water (Delta(18)O) and carbon isotope discrimination (Delta(13)C) in the same pooled leaves and in mature kernels. Second-year water use was evaluated by measuring leaf temperature, g(s) and relative water content (RWC). *Within each growing condition, hybrids showed higher F(s), mineral accumulation, RWC, and lower leaf temperature, Delta(18)O and Delta(13)C than inbred lines. Therefore, hybrids had a better water status than inbred lines, regardless of the water conditions. Differences in grain yield across growing conditions were explained by differences in water-use traits, with hybrids and inbred lines following a common pattern. Within each growing condition, most variations in grain yield, between hybrids and inbred lines, were also explained by differences in plant water-use traits. *Heterosis in tropical maize seems to be mediated by improved water use, irrespective of the water conditions during growth.
Araus
José Luis
JL
International Maize and Wheat Improvement Center (CIMMYT), El Batán, Mexico.|Unitat de Fisiologia Vegetal, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain.
Sánchez
Ciro
C
International Maize and Wheat Improvement Center (CIMMYT), El Batán, Mexico.
Cabrera-Bosquet
Llorenç
L
International Maize and Wheat Improvement Center (CIMMYT), El Batán, Mexico.|Unitat de Fisiologia Vegetal, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain.
D000388:Air; D018533:Biomass; D002734:Chlorophyll / Q000378:metabolism; D018556:Crops, Agricultural / Q000254:growth & development; D003681:Dehydration; D004777:Environment; D006823:Hybrid Vigor / Q000235:genetics*; D006824:Hybridization, Genetic; D007178:Inbreeding; D009584:Nitrogen / Q000378:metabolism; D019655:Quantitative Trait, Heritable; D013696:Temperature; D014867:Water / Q000378:metabolism*; D003313:Zea mays / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism*
D014867:Water; D002734:Chlorophyll; D009584:Nitrogen
Ahmadzadeh A, Lee EA, Tollenaar M. 2004. Heterosis for leaf CO2 exchange rate during the grain-filling period in maize. Crop Science 44: 2095-2100.
Andrade FH, Cirilo AG, Echarte L. 2000. Factors affecting kernel number in maize. In: Otegui ME, Slafer GA, eds. Chapter 5 Physiological bases for maize improvement. Binghampton New York, NY, USA: Food Product Press an imprint of the Harworth Press, Inc, 59-74.
Andrews JR, Bredenkamp GJ, Baker NR. 1993. Evaluation of the role of state transitions in determining the efficiency of light utilisation for CO2 assimilation in leaves. Photosynthesis Research 38: 15-26.
Araus JL, Amaro T, Casadesus J, Asbati A, Nachit MM. 1998. Relationships between ash content, carbon isotope discrimination and yield in durum wheat. Australian Journal of Plant Physiology 25: 835-842.
Araus JL, Casadesus J, Asbati A, Nachit MM. 2002a. Basis of the relationship between ash content in the flag leaf and carbon isotope discrimination in kernels of durum wheat. Photosynthetica 39: 591-596.
Araus JL, Slafer GA, Reynolds MP, Royo C. 2002b. Plant breeding and water relations in C3 cereals: what should we breed for? Annals of Botany 89: 925-940.
Araus JL, Slafer GA, Royo C, Serret MD. 2008. Breeding for yield potential and stress adaptation in cereals. Critical Reviews in Plant Science 27: 377-412.
Ashby E. 1930. Studies in the inheritance of physiological characters I. A physiological investigation of the nature of hybrid vigour in maize. Annals of Botany 44: 457-468.
Ashby E. 1932. Studies in the inheritance of physiological characters II. Further experiments upon the basis of hybrid vigour and upon the inheritance of efficiency index and respiration rate in maize. Annals of Botany 46: 1007-1032.
Bänziger M, Edmeades GO, Beck D, Bellon M. 2000. Breeding for drought and nitrogen stress tolerance in maize: from theory to practice. Mexico D.F., Mexico: CIMMYT.
Bänziger M, Lafitte HR. 1997. Efficiency of secondary traits for improving maize for low-nitrogen target environments. Crop Science 37: 110-1117.
Barbour MM. 2007. Stable oxygen isotope composition of plant tissue: a review. Functional Plant Biology 34: 83-94.
Barbour MM, Fischer RA, Sayre KD, Farquhar GD. 2000. Oxygen isotope ratio of leaf and grain material correlates with stomatal conductance and grain yield in irrigated wheat. Australian Journal of Plant Physiology 27: 625-637.
Betrán FJ, Beck D, Bänziger M, Edmeades GO. 2003a. Secondary traits in parental inbreds and hybrids under stress and non-stress environments in tropical maize. Field Crops Research 83: 51-65.
Betrán FJ, Beck D, Bänziger M, Edmeades GO. 2003b. Genetic analysis of inbred and hybrid grain yield under stress and non-stress environments in tropical maize. Crop Science 43: 807-817.
Betrán FJ, Menz M, Bänzinger M. 2004. Corn breeding. In: Smith CW, Betrán FJ, Runge ECA, eds. Corn: Origin, history, technology, and production. Hoboken, NJ, USA: John Wiley & Sons, 305-398.
Betrán FJ, Ribaut JM, Beck D, Gonzalez de Leon D. 2003c. Genetic diversity, specific combining ability, and heterosis in tropical maize under stress and nonstress environments. Crop Science 43: 797-806.
Blackman VH. 1919. The compound interest law and plant growth. Annals of Botany (London) 33: 353-360.
Blum A. 1997. Constitutive traits affecting plant performance under stress. In: Edmeades GO, Bänziger M, Mickelson HR, Peña-Valdivia CB, eds. Developing drought and low-N tolerant maize. El Batan, Mexico: CIMMYT, 131-135.
Blum A. 2005. Drought resistance, water-use efficiency, and yield potential - are they compatible, dissonant, or mutually exclusive? Australian Journal of Agricultural Research 56: 1159-1168.
Blum A. 2009. Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crops Research 112: 119-123.
Bolaños J, Edmeades GO. 1996. The importance of the anthesis-silking interval in breeding for drought tolerance in tropical maize. Field Crops Research 48: 65-80.
Bruce WB, Edmeades GO, Barker TC. 2002. Molecular and physiological approaches to maize improvement for drought tolerance. Journal of Experimental Botany 53: 13-25.
Cabrera-Bosquet L, Molero G, Nogués S, Araus JL. 2009c. Water and nitrogen conditions affect the relationships of Δ13C and Δ18O to gas exchange and growth in durum wheat. Journal of Experimental Botany 60: 1633-1644.
Cabrera-Bosquet L, Sánchez C, Araus JL. 2009a. Oxygen isotope enrichment (Δ18O) reflects yield potential and drought resistance in maize. Plant, Cell & Environment 32: 1487-1499.
Cabrera-Bosquet L, Sánchez C, Araus JL. 2009b. How yield relates to ash content, Δ13C and Δ18O in maize grown under different water regimes. Annals of Botany 104: 1207-1216. 10.1093/aob/mcp229
Chapman SC, Edmeades GO. 1999. Selection improves drought tolerance in tropical maize populations. II. Direct and correlated responses among secondary traits. Crop Science 39: 1315-1324.
Chimenti CA, Matías M, Hall AJ. 2006. Divergent selection for osmotic adjustment results in improved drought tolerance in maize (Zea mays L.) in both early growth and flowering phase. Field Crops Research 95: 305-315.
Chun L, Mi G, Li J, Chen F, Zhang F. 2005. Genetic analysis of maize root characteristics in response to low nitrogen stress. Plant and Soil 276: 369-382.
Dercon G, Clymans E, Diels J, Merckx R, Deckers J. 2006. Differential 13C isotopic discrimination in maize at varying water stress and at low to high nitrogen availability. Plant and Soil 282: 313-326.
Ding L, Wang KJ, Jiang GM, Li YG, Jiang CD, Liu MZ, Niu SL, Peng Y. 2006. Diurnal variation of gas exchange, chlorophyll fluorescence, and xanthophyll cycle components of maize hybrids released in different years. Photosynthetica 44: 26-31.
Echarte L, Andrade FH, Vega CRC, Tollenaar M. 2004. Kernel number determination in Argentinean maize hybrids re- between 1965 and 1993. Crop Science 44: 1654-1661.
Farquhar GD, Cernusak LA, Barnes B. 2007. Heavy water fractionation during transpiration. Plant Physiology 143: 11-18.
Farquhar GD, Ehleringer JR, Hubick K. 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40: 503-537.
Ferrio JP, Mateo MA, Bort J, Abdalla O, Voltas J, Araus JL. 2007. Relationships of grain δ13C and δ18O with wheat phenology and yield under water-limited conditions. Annals of Applied Biology 150: 207-215.
Flexas J, Escalona JM, Evain S, Gulias J, Moya I, Osmond CB, Medrano H. 2002. Steady-state chlorophyll fluorescence (Fs) measurements as a tool to follow variations of net CO2 assimilation and stomatal conductance during water-stress in C3 plants. Physiologia Plantarum 114: 231-240.
Flexas J, Escalona JM, Medrano H. 1999. Water stress induces different levels of photosynthesis and electron transport rate regulations in grapevines. Plant, Cell & Environment 22: 39-48.
Hochholdinger F, Woll K, Sauer M, Dembinsky D. 2004. Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Annals of Botany 93: 359-368.
Hoecker N, Keller B, Muthreich N, Chollet D, Descombes P, Piepho HP, Hochholdinger F. 2008. Comparison of maize (Zea mays L.) F1-Hybrid and parental inbred line primary root transcriptomes suggests organ-specific patterns of nonadditive gene expression and conserved expression trends. Genetics 179: 1275-1283.
Hoecker N, Keller B, Piepho HP, Hochholdinger F. 2006. Manifestation of heterosis during early maize (Zea mays L.) root development. Theoretical and Applied Genetics 112: 421-429.
Hsiao TC. 1973. Plant responses to water stress. Annual Review of Plant Physiology 24: 519-570.
Inman D, Khosla R, Reich RM, Westfall DG. 2008. Normalized difference vegetation index and soil color-based management zones in irrigated maize. Agronomy Journal 100: 60-66.
Jiang Q, Roche D, Monaco TA, Hole D. 2006. Stomatal conductance is a key parameter to assess limitations to photosynthesis and growth potential in barley genotypes. Plant Biology 8: 515-521.
Kramer PJ, Boyer JS. 1995. Water relations of plants and soils. San Diego, CA, USA: Academic Press Inc.
Lemcoff JH, Chimenti CA, Daveza TAE. 1998. Osmotic adjustment in maize (Zea mays L.): changes with ontogeny and its relationship with phenotypic stability. Journal of Agronomy and Crop Science 180: 241-247.
Li B, Tian X-L, Wang G-W, Pan F, Li Z-H. 2008. Heterosis of root growth in maize (Zea mays L.) seedlings under water stress. Acta Agronomica Sinica 34: 662-668.
Liang GH, Reddy CR, Dayton AD. 1972. Heterosis, inbreeding depression, and heritability estimates in a systematic series of grain sorghum genotypes. Crop Science 12: 409-411.
Liu W, Tollenaar M. 2009a. Physiological mechanisms underlying heterosis for shade tolerance in maize. Crop Science 49: 1817-1826.
Liu W, Tollenaar M. 2009b. Response of yield heterosis to increasing plant density in maize. Crop Science 49: 1807-1816.
Liu X-F, Zhang S-Q, Yang X-Q, Shan L. 2009. Heterosis of water uptake ability by roots of maize at cell level. Acta Agronomica Sinica 35: 1546-1551.
Marti J, Bort J, Slafer GA, Araus JL. 2007. Can wheat yield be assessed by early measurements of NDVI? Annals of Applied Biology 150: 253-257.
Medrano H, Escalona JM, Bota J, Gulias J, Flexas J. 2002. Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Annals of Botany 89: 895-905.
Meyer S, Pospisil H, Scholten S. 2007. Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern. Plant Molecular Biology 63: 381-391.
Monneveux P, Sánchez C, Tiessen A. 2008. Future progress in drought tolerance in maize needs new secondary traits and cross combinations. Journal of Agricultural Science 146: 1-14.
Monneveux P, Sheshshayee MS, Akhter J, Ribaut JM. 2007. Using carbon isotope discrimination to select maize (Zea mays L.) inbred lines and hybrids for drought tolerance. Plant Science 173: 390-396.
Pandey S, Diallo AO, Islam TMT, Deutsch J. 1986. Progress from selection in eight tropical maize populations using international testing. Crop Science 26: 879-884.
Paschold A, Marcon C, Hoecker N, Hochholdinger F. 2010. Molecular dissection of heterosis manifestation during early maize root development. Theoretical and Applied Genetics 120: 383-388.
Passioura J. 1996. Drought and drought tolerance. Plant Growth Regulation 20: 79-83.
Ritchie SW, Hanway JJ, Benson GO. 1993. How a corn plant develops. Special Report No48. Iowa State University of Science and technology, Cooperative Extension Service Ames, Iowa, USA.
Rood SB, Buzzell RI, Mander LN, Pearce D, Pharis RP. 1988. Gibberellins: a phytohormonal basis for heterosis in maize. Science 241: 1216-1218.
Sinha SK, Khanna R. 1975. Physiological, biochemical, and genetic basis of heterosis. Advances in Agronomy 27: 123-174.
Smith SN. 1934. Response of inbred lines and crosses in maize to variations of nitrogen and phosphorus supplied as nutrients. American Society of Agronomy 26: 785-804.
Tardieu F. 2006. Leaf growth under water-limited conditions. In: Ribaut JM, ed. Drought adaptation in cereals. New York, NY, USA: The Harworth Press, Inc, 145-169.
Teal RK, Tubana B, Girma K, Freeman KW, Arnall DB, Walsh O, Raun WR. 2006. In-season prediction of corn grain yield potential using normalized difference vegetation index. Agronomy Journal 98: 1488-1494.
Tollenaar M, Ahmadzadeh A, Lee EA. 2004. Physiological basis of heterosis for grain yield in maize. Crop Science 44: 2086-2094.
Tollenaar M, Lee EA. 2006. Dissection of physiological processes underlying grain yield in maize by examining genetic improvement and heterosis. Maydica 51: 399-408.
Valentinuz OR, Tollenaar M. 2004. Vertical profile of leaf senescence during the grain-filling period in older and newer maize hybrids. Crop Science 44: 827-834.