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QTL mapping of root aerenchyma formation in seedlings of a maize × rare teosinte “Zea nicaraguensis” cross

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Abstract

Using a 141 F2 population generated from maize inbred B64 × teosinte Zea nicaraguensis cross, quantitative trait loci (QTLs) controlling aerenchyma formation in roots under non-flooding drained soil conditions were identified. Seedlings of Z. nicaraguensis formed clear aerenchyma in the cortex of adventitious roots in non-flooding conditions, whereas the maize inbred line B64 did not. In the F2 population, the capacity to develop aerenchyma exhibited wide and continuous variation, suggesting the trait was controlled by multiple genes. A linkage map was developed using 85 SSR markers, covering 1,224 cM across all ten chromosomes. Composite interval mapping analysis revealed that four QTLs for aerenchyma formation under non-flooding conditions were located to two regions of chromosome 1 (identified as Qaer1.02-3 and Qaer1.07), chromosome 5 (Qaer5.09) and chromosome 8 (Qaer8.06-7), and these explained 46.5% of the total phenotypic variance. The multiple interval mapping approach identified additional QTLs on chromosomes 1 (Qaer1.01) and 5 (Qaer5.01). Using these results, it may be possible to use SSR markers linked to aerenchyma formation in a marker assisted selection approach to introduce aerenchyma formation in drained soil conditions into maize for the eventual development of flooding tolerant maize hybrids.

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References

  • Arikado H, Adachi Y (1955) Anatomical and ecological responses of barley and some forage crops to the flooding treatment. Bull Fac Agric Mie Univ 11:1–29

    Google Scholar 

  • Armstrong W, Justin SHFW, Beckett PM, Lythe S (1991) Root adaptation to soil waterlogging. Aquat Bot 39:57–73

    Article  Google Scholar 

  • Barcelo J, Guevara P, Poschenrieder Ch (1993) Silicon amelioration of aluminium toxicity in teosinte (Zea mays L. ssp. mexicana). Plant Soil 154:249–255

    Article  CAS  Google Scholar 

  • Bird R McK (2000) A remarkable new teosinte from Nicaragua: growth and treatment of progeny. Maize Gen Coop Newsl 74:58–59

    Google Scholar 

  • Bomblies K, Doebley JF (2006) Pleiotropic effects of the duplicate maize FLORICAULA/LEAFY genes zfl1 and zfl2 on traits under selection during maize domestication. Genetics 172:519–531

    Article  PubMed  CAS  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Burdick DM (1989) Root aerenchyma development in Spartina patens in response to flooding. Am J Bot 76:777–780

    Article  Google Scholar 

  • Cohen JI, Galinat WC (1984) Potential use of alien germplasm for maize improvement. Crop Sci 24:1011–1015

    Article  Google Scholar 

  • Colmer TD (2003) 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

    Article  PubMed  CAS  Google Scholar 

  • Doebley J, Stec A (1991) Genetic-analysis of the morphological differences between maize and teosinte. Genetics 129:285–295

    PubMed  CAS  Google Scholar 

  • Doebley J, Stec A (1993) Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics 134:559–570

    PubMed  CAS  Google Scholar 

  • Drew MC, Jackson MB, Giffard S (1979) Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) in root may be adaptive responses to flooding in Zea mays L. Planta 147:83–88

    Article  CAS  Google Scholar 

  • Eubanks MW (1997) Molecular analysis of crosses between Tripsacum dactyloides and Zea diploperennis (Poaceae). Theor Appl Genet 94:707–712

    Article  CAS  Google Scholar 

  • Evans DE (2004) Aerenchyma formation. New Phytol 161:35–49

    Article  Google Scholar 

  • Harlan JR (1976) Genetic resources in wild relatives of crops. Crop Sci 16:329–333

    Article  Google Scholar 

  • Hoisington D, Khairallah M, Reeves T, Ribaut J-M, Skovmand B, Taba S, Warburton M (1999) Plant genetic resources: what can they contribute toward increased crop productivity? Proc Natl Acad Sci USA 96:5937–5943

    Article  PubMed  CAS  Google Scholar 

  • Iltis HH, Benz BF (2000) Zea nicaraguensis (Poaceae), a new teosinte from Pacific coastal Nicaragua. Novon 10:382–390

    Article  Google Scholar 

  • Iltis HH, Doebley JF (1980) Taxonomy of Zea (Gramineae). II Subspecific categories in the Zea mays complex and a generic synopsis. Am J Bot 67:994–1004

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jackson MB, Armstrong W (1999) Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biol 1:274–287

    CAS  Google Scholar 

  • Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytol 106:465–495

    Google Scholar 

  • Justin SHFW, Armstrong W (1991) Evidence for the involvement of ethene in aerenchyma formation in adventitious roots of rice (Oryza sativa L.). New Phytol 118:49–62

    Article  CAS  Google Scholar 

  • Kao C-H, Zeng Z-B, Teasdale RD (1999) Multiple interval mapping for quantitative trait loci. Genetics 152:1203–1216

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Komatsuda T, Nakamura I, Takaiwa F, Oka S (1998) Development of STS markers closely linked to the vrs1 locus in barley, Hordeum vulgare. Genome 41:680–685

    Article  CAS  Google Scholar 

  • Konings H (1982) Ethylene-promoted formation of aerenchyma in seedling roots of Z mays L. under aerated and non-aerated conditions. Physiol Plant 54:119–124

    Article  CAS  Google Scholar 

  • Laan P, Berrevoets MJ, Lythe S, Armstrong W, Blom CWPM (1989) Root morphology and aerenchyma formation as indicators of the flooding-tolerance of Rumex species. J Ecol 77:693–703

    Article  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Lizaso JI, Melendez LM, Ramirez R (2001) Early flooding of two cultivars of tropical maize I. shoot and root growth. J Plant Nutr 24:979–995

    Article  CAS  Google Scholar 

  • Lu H, Romero-Severson J, Bernardo R (2002) Chromosomal regions associated with segregation distortion in maize. Theor Appl Genet 105:622–628

    Article  PubMed  CAS  Google Scholar 

  • Mano Y, Muraki M, Komatsu T, Fujimori M, Akiyama F, Takamizo T (2002) Varietal difference in pre-germination flooding tolerance and waterlogging tolerance at the seedling stage in maize inbred accessions. Jpn J Crop Sci 71:361–367

    Google Scholar 

  • Mano Y, Muraki M, Fujimori M, Takamizo T, Kindiger B (2005a) Identification of QTL controlling adventitious root formation during flooding conditions in teosinte (Zea mays ssp. huehuetenangensis) seedlings. Euphytica 142:33–42

    Article  Google Scholar 

  • Mano Y, Muraki M, Fujimori M, Takamizo T, Kindiger B (2005b) AFLP-SSR maps of maize x teosinte and maize x maize: comparison of map length and segregation distortion. Plant Breed 124:432–439

    Article  CAS  Google Scholar 

  • Mano Y, Omori F, Muraki M, Takamizo T (2005c) QTL mapping of adventitious root formation during flooding conditions in tropical maize (Zea mays L.) seedlings. Breed Sci 55:343–347

    Article  Google Scholar 

  • Mano Y, Muraki M, Takamizo T (2006a) Identification of QTL controlling waterlogging tolerance in reducing soil conditions in maize (Zea mays L.) seedlings. Plant Prod Sci 9:176–181

    Article  CAS  Google Scholar 

  • Mano Y, Omori F, Takamizo T, Kindiger B, Bird R McK Loaisiga CH (2006b) Variation for root aerenchyma formation in flooded and non-flooded maize and teosinte seedlings. Plant Soil 281:269–279

    Article  CAS  Google Scholar 

  • McDonald MP, Galwey NW, Colmer TD (2001) Waterlogging tolerance in the tribe Triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss. Plant Cell Environ 24:585–596

    Article  Google Scholar 

  • Molina MC, Naranjo CA (1987) Cytogenetic studies in the genus Zea. 1. Evidence for five as the basic chromosome number. Theor Appl Genet 73:542–550

    Article  Google Scholar 

  • Nakazono M, Qiu F, Borsuk LA, Schnable PS (2003) Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell 15:583–596

    Article  PubMed  CAS  Google Scholar 

  • Pezeshki SR (2001) Wetland plant responses to soil flooding. Environ Exp Bot 46:299–312

    Article  Google Scholar 

  • Ponnamperuma FN (1984) Effects of flooding on soils. In: Kozlowski TT (ed) Flooding and plant growth. Academic Press, Orlando, FL, USA, pp 9–45

    Google Scholar 

  • Ray JD, Kindiger B, Sinclair TR (1999) Introgressing root aerenchyma into maize. Maydica 44:113–117

    Google Scholar 

  • Reeves RG (1950) The use of teosinte in the improvement of corn inbreds. Agron J 42:248–251

    Article  Google Scholar 

  • Rogers JS (1950) The inheritance of photoperiodic response and tillering in maize-teosinte hybrids. Genetics 35:513–540

    PubMed  CAS  Google Scholar 

  • Sachs MM, Sabbaiah CC, Saab IN (1996) Anaerobic gene expression and flooding tolerance in maize. J Exp Bot 47:1–15

    Article  CAS  Google Scholar 

  • Schussler EE, Longstreth DJ (1996) Aerenchyma develops by cell lysis in roots and cell separation in leaf petioles in Sagittaria lancifolia (Alismataceae). Am J Bot 83:1266–1273

    Article  Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Google Scholar 

  • Sharopova N, McMullen MD, Schultz L, Schroeder S, Sanchez-Villeda H, Gardiner J, Bergstrom D, Houchins K, Melia-Hancock S, Musket T, Duru N, Polacco M, Edwards K, Ruff T, Register JC, Brouwer C, Thompson R, Velasco R, Chin E, Lee M, Woodman-Clikeman W, Long MJ, Liscum E, Cone K, Davis G, Coe EH (2002) Development and mapping of SSR markers for maize. Plant Mol Biol 48:463–481

    Article  PubMed  CAS  Google Scholar 

  • Siangliw M, Toojinda T, Tragoonrung S, Vanavichit A (2003) Thai jasmine rice carrying QTLch9 (SubQTL) in submergence tolerant. Ann Bot 91:255–261

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N, Crawford RMM (1983) Variation in the structure and response to flooding of root aerenchyma in some wetland plants. Ann Bot 51:237–249

    Google Scholar 

  • Stanca AM, Romagosa I, Takeda K, Lundborg T, Terzi V, Cattivelli L (2003) Diversity in abiotic stress tolerances. In: Von Bothmer R, van Hintum Th, Knüpffer H, Sato K (eds) Diversity in Barley (Hordeum vulgare). Elsevier Science B.V. Amsterdam, p 280

  • Statistic Department, Minister’s Secretariat, Ministry of Agriculture, Forestry and Fisheries (2005) Section VIII crops, 8 feed and forage crops. In: Statistic Department, Minister’s Secretariat, Ministry of Agriculture, Forestry and Fisheries (eds) The 79th statistical yearbook of ministry of agriculture forestry and fisheries, 2003–2004. Tokyo Japan, p 205

  • Stuber CW, Edwards MD, Wendel JF (1987) Molecular marker-facilitated investigations of quantitative trait loci in maize. II. Factors influencing yield and its component traits. Crop Sci 27:639–648

    Article  Google Scholar 

  • Subbaiah CC, Sachs MM (2003) Molecular and cellular adaptations of maize to flooding stress. Ann Bot 91:119–127

    Article  PubMed  CAS  Google Scholar 

  • Takeda K (1989) Varietal variation of flooding tolerance in barley seedlings, and its diallel analysis. Jpn J Breed 39(Suppl 1):174–175

    Google Scholar 

  • Ting YC (1958) Inversions and other characteristics of teosinte chromosomes. Cytologia 23:239–250

    Google Scholar 

  • Visser EJW, Bogemann GM, Blom CWPM, Voesenek LACJ (1996) Ethylene accumulation in waterlogged Rumex plants promotes formation of adventitious roots. J Exp Bot 47:403–410

    Article  CAS  Google Scholar 

  • Wang S, Basten CJ, Zeng Z-B (2006) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC, USA. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm

  • Westerbergh A, Doebley J (2002) Morphological traits defining species differences in wild relatives of maize are controlled by multiple quantitative trait loci. Evolution 56:273–283

    PubMed  Google Scholar 

  • Xu K, Xu X, Ronald PC, Mackill DJ (2000) A high-resolution linkage map of the vicinity of the rice submergence tolerance locus Sub1. Mol Gen Genet 263:681–689

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki T (1952) Studies on the excess-moisture injury of upland crops in overmoist soil from the viewpoint of soil chemistry and plant physiology. Bull Natl Inst Agric Sci B1:1–92

    Google Scholar 

  • Zeng Z-B, Kao C-H, Basten CJ (1999) Estimating the genetics architecture of quantitative traits. Genet Res 74:279–289

    Article  PubMed  CAS  Google Scholar 

  • Zeng Z-B, Liu J, Stam LF, Kao C-H, Marcer JM, Laurie CC (2000) Genetic architecture of a morphological shape difference between two Drosophila species. Genetics 154:299–310

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to the International Maize and Wheat Improvement Center (CIMMYT), Mexico for providing seed of Z. nicaraguensis, the Gene Bank, National Institute of Agrobiological Sciences, Tsukuba, Japan for supplying seed of B64, and the Corn and Sorghum Breeding laboratory, National Institute of Livestock and Grassland Science, Nasushiobara, Japan for supporting this work. We thank Dr. K. Takeda (Research Institute for Bioresources, Okayama University, Kurashiki, Japan), Dr. T. Komatsuda (National Institute of Agrobiological Sciences, Tsukuba, Japan), and Dr. M. Nakazono (University of Tokyo, Bunkyo-ku, Japan) for critically reviewing the manuscript.

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Mano, Y., Omori, F., Takamizo, T. et al. QTL mapping of root aerenchyma formation in seedlings of a maize × rare teosinte “Zea nicaraguensis” cross. Plant Soil 295, 103–113 (2007). https://doi.org/10.1007/s11104-007-9266-9

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