Skip to main content
SpringerLink
Log in

A non-additive interaction in a single locus causes a very short root phenotype in wheat

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Non-additive allelic interactions underlie over dominant and under dominant inheritance, which explain positive and negative heterosis. These heteroses are often observed in the aboveground traits, but rarely reported in root. We identified a very short root (VSR) phenotype in the F1 hybrid between the common wheat (Triticum aestivum L.) landrace Chinese Spring and synthetic wheat accession TA4152-71. When germinated in tap water, primary roots of the parental lines reached ~15 cm 10 days after germination, but those of the F1 hybrid were ~3 cm long. Selfing populations segregated at a 1 (long-root) to 1 (short-root) ratio, indicating that VSR is controlled by a non-additive interaction between two alleles in a single gene locus, designated as Vsr1. Genome mapping localized the Vsr1 locus in a 3.8-cM interval delimited by markers XWL954 and XWL2506 on chromosome arm 5DL. When planted in vermiculite with supplemental fertilizer, the F1 hybrid had normal root growth, virtually identical to the parental lines, but the advanced backcrossing populations segregated for VSR, indicating that the F1 VSR expression was suppressed by interactions between other genes in the parental background and the vermiculite conditions. Preliminary physiological analyses showed that the VSR suppression is independent of light status but related to potassium homeostasis. Phenotyping additional hybrids between common wheat and synthetics revealed a high VSR frequency and their segregation data suggested more Vsr loci involved. Because the VSR plants can be regularly maintained and readily phenotyped at the early developmental stage, it provides a model for studies of non-additive interactions in wheat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alemán F, Nieves-Cordones M, Martίnez V, Rubio F (2011) Root K+ acquisition in plants: the Arabidopsis thaliana Model. Plant Cell Physiol 52(9):1603–1612

    Article  PubMed  Google Scholar 

  • Bateson W (1909) Heredity and variation in modern lights. In: Seward AC (ed) Darwin and modern science. Cambridge University Press, Cambridge, pp 85–101

    Google Scholar 

  • Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8(5):382–393

    Article  PubMed  CAS  Google Scholar 

  • Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D (2007) Autoimmune response as a mechanism for a Dobzhansky–Muller-type incompatibility syndrome in plants. PLoS Biol 5(9):e236

    Article  PubMed  Google Scholar 

  • Boursiac Y, Lee SM, Romanowsky S, Blank R, Sladek C, Chung WS, Harper JF (2011) Disruption of the vacuolar calcium-ATPases in Arabidopsis results in the activation of a salicylic acid-dependent programmed cell death pathway. Plant Physiol 154(3):1158–1171

    Article  Google Scholar 

  • Brieger F (1929) Vererbung bei Artbastarden unter besonderer berücksichtigung der Gattung Nicotiana. Der Züchter 1:140–152

    Google Scholar 

  • Canvin DT, McVetty PBE (1976) Hybrid grass-clump dwarfness in wheat: physiology and genetics. Euphytica 25:471–483

    Article  Google Scholar 

  • Chen J, Ding J, Ouyang Y, Du H, Yang J, Cheng K, Zhao J, Qiu S, Zhang X, Yao J, Liu K, Wang L, Xu C, Li X, Xue Y, Xia M, Ji Q, Lu J, Xu M, Zhang Q (2008) A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica-japonica hybrids in rice. Proc Natl Acad Sci USA 105:11436–11441

    Article  PubMed  CAS  Google Scholar 

  • Chin K, Moeder W, Yoshioka K (2009) Biological roles of cyclic-nucleotide-gated ion channels in plants: what we know and don’t know about this 20 member ion channel family. Botany 87:668–677

    Article  CAS  Google Scholar 

  • Christian M, Steffens B, Schenck D, Burmester S, Böttger M, Lüthen H (2006) How does auxin enhance cell elongation? Roles of auxin-binding proteins and potassium channels in growth control. Plant Biol (Stuttg) 8(3):346–352

    Article  CAS  Google Scholar 

  • Chu YE, Oka H (1972) The distribution and effects of genes causing F1weakness in Oryza breviligulata and O. glaberrima. Genetics 70(1):163–173

    PubMed  CAS  Google Scholar 

  • Chu CG, Faris JD, Friesen TL, Xu SS (2006) Molecular mapping of hybrid necrosis genes Ne1 and Ne2 in hexaploid wheat using microsatellite markers. Theor Appl Genet 112(7):1374–1381

    Article  PubMed  CAS  Google Scholar 

  • Dilkes BP, Spielman M, Weizbauer R, Watson B, Burkart-Waco D, Scott RJ, Comai L (2008) The maternally expressed WRKY transcription factor TTG2 controls lethality in interploidy crosses of Arabidopsis. PLoS Biol 6(12):e308

    Article  Google Scholar 

  • Dvorak J, Luo M, Deal KR, McGuire P, You F, Gu YQ, Anderson O, Li W, Sehgal SS, Gill BS, Stein J, Pasternak S, Ware D, McCombie WR, Martis MM, Mayer K, Dolezel J (2012) Physical map and shotgun sequence of the Aegilops tauschii genome. Plant and Animal Genome Conference XX (https://pag.confex.com/pag/xx/webprogram/Paper2057.html)

  • Faris JD, Laddomada B, Gill BS (1998) Molecular mapping of segregation distortion loci in Aegilops tauschii. Genetics 149:319–327

    PubMed  CAS  Google Scholar 

  • Groszmann M, Greaves IK, Albertyn ZI, Scofield GN, Peacock WJ, Dennis ES (2011) Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc Natl Acad Sci USA 108:2617–2622

    Article  PubMed  CAS  Google Scholar 

  • Ha M, Lu J, Tian L, Ramachandran V, Kasschau KD, Chapman EJ, Carrington JC, Chen X, Wang XJ, Chen ZJ (2009) Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci USA 106:17835–17840

    Article  PubMed  CAS  Google Scholar 

  • Hermsen JGT (1963) The genetic basis of hybrid necrosis in wheat. Genetica 33:245–287

    Article  Google Scholar 

  • Heyne EG, Wiebe GA, Painter RH (1943) Complementary genes in wheat causing death of F1 plants. J Hered 34:243–245

    Google Scholar 

  • Jeuken MJ, Zhang NW, McHale LK, Pelgrom K, den Boer E, Lindhout P, Michelmore RW, Visser RG, Niks RE (2009) Rin4 causes hybrid necrosis and race-specific resistance in an interspecific lettuce hybrid. Plant Cell 21(10):3368–3378

    Article  PubMed  CAS  Google Scholar 

  • Kihara H (1944) Discovery of the DD-analyzer, one of the ancestors of Triticum vulgare. Agric Hort (Tokyo) 19:13–14

    Google Scholar 

  • Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12(3):172–175

    Google Scholar 

  • Krieger U, Lippman ZB, Zamir D (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat Genet 42:459–463

    Google Scholar 

  • Krüger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L, Jones JD (2002) A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296(5568):744–747

    Article  PubMed  Google Scholar 

  • Kumar S, Gill BS, Faris JD (2007) Identification and characterization of segregation distortion loci along chromosome 5B in tetraploid wheat. Mol Genet Genomics 278:187–196

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1(2):174–181

    Article  PubMed  CAS  Google Scholar 

  • Li W, Huang L, Gill BS (2008) Recurrent deletions of puroindoline genes at the grain hardness locus in four independent lineages of polyploid wheat. Plant Physiol 146(1):200–212

    Article  PubMed  CAS  Google Scholar 

  • Long Y, Zhao L, Niu B, Su J, Wu H, Chen Y, Zhang Q, Guo J, Zhuang C, Mei M, Xia J, Wang L, Wu H, Liu YG (2008) Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci U S A. 105(48):18871–18876

    Article  PubMed  CAS  Google Scholar 

  • Maan SS, Carlson KM, Williams ND, Yang T (1987) Chromosomal arm location and gene-centromere distance of a dominant gene for male sterility in wheat. Crop Sci 27:494–500

    Article  Google Scholar 

  • McFadden ES, Sears ER (1946) The origin of Triticum spelta and its free-threshing hexaploid relatives. J Hered 37:81–89

    PubMed  Google Scholar 

  • McIntosh RA, Yamazaki Y, DubcovskY J, Rogers J, Morris C, Somers DJ, Appels R, Devos KM (2008) Catalogue of gene symbols for wheat. In: Proceedings of the 11th international wheat genetics symposium, 24–29 August 2008, Brisbane Qld Australia. http://wheat.pw.usda.gov/GG2/Triticum/wgc/2008/Catalogue2008.pdf

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8(11):1113–1130

    PubMed  CAS  Google Scholar 

  • Miranda LM, Murphy JP, Marshall D, Leath S (2006) Pm34: a new powdery mildew resistance gene transferred from Aegilops tauschii Coss. to common wheat (Triticum aestivum L.). Theor Appl Genet 13(8):1497–1504

    Article  Google Scholar 

  • Mizuno N, Hosogi N, Park P, Takumi S (2010) Hypersensitive response-like reaction is associated with hybrid necrosis in interspecific crosses between tetraploid wheat and Aegilops tauschii coss. PLoS ONE 5(6):e11326

    Article  PubMed  Google Scholar 

  • Mizuno N, Shitsukawa N, Hosogi N, Park P, Takumi S (2011) Autoimmune response and repression of mitotic cell division occur in inter-specific crosses between tetraploid wheat and Aegilops tauschii Coss. that show low temperature-induced hybrid necrosis. Plant J 68(1):114–128

    Article  PubMed  CAS  Google Scholar 

  • Peng J, Korol AB, Fahima T, Röder MS, Ronin YI, Li YC, Nevo E (2000) Molecular genetic maps in wild emmer wheat, Triticum dicoccoides: genome-wide coverage, massive negative interference, and putative quasi-linkage. Genome Res 10:1509–15031

    Article  PubMed  CAS  Google Scholar 

  • Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590

    Article  PubMed  CAS  Google Scholar 

  • Pukhalskiy VA, Martynov SP, Dobrotvorskaya TV (2000) Analysis of geographical and breeding-related distribution of hybrid necrosis genes in bread wheat (Triticum aestivum L.). Euphytica 114:233–240

    Article  CAS  Google Scholar 

  • Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Akhunov ED, Dvorak J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Kantety R, La Rota CM, Munkvold JD, Sorrells SF, Sorrells ME, Dilbirligi M, Sidhu D, Erayman M, Randhawa HS, Sandhu D, Bondareva SN, Gill KS, Mahmoud AA, Ma X-F, Miftahudin, Gustafson JP, Wennerlind EJ, Nduati V, Gonzalez-Hernandez JL, Anderson JA, Peng JH, Lapitan NLV, Hossain KG, Kalavacharla V, Kianian SF, Pathan MS, Zhang DS, Nguyen HT, Choi D-W, Close TJ, McGuire PE, Qualset CO, Gill BS (2004) A chromosome bin map of 10,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

    Article  PubMed  CAS  Google Scholar 

  • Sassi M, Lu Y, Zhang Y, Wang J, Dhonukshe P, Blilou I, Dai M, Li J, Gong X, Jaillais Y, Yu X, Traas J, Ruberti I, Wang H, Scheres B, Vernoux T, Xu J (2012) COP1 mediates the coordination of root and shoot growth by light through modulation of PIN1- and PIN2-dependent auxin transport in Arabidopsis. Development 139(18):3402–3412

    Article  PubMed  CAS  Google Scholar 

  • Sears ER (1966) Nullisomic-tetrasomic combinations in hexaploid wheat. In: Riley R, Lewis KR (eds) Chromosome manipulation and plant genetics. Oliver and Boyd, Edinburgh, pp 29–45

    Google Scholar 

  • Shivaprasad PV, Dunn RM, Santos BACM, Bassett A, Baulcombe DC (2012) Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J 31:257–266

    Article  CAS  Google Scholar 

  • Smith LM, Bomblies K, Weigel D (2011) Complex evolutionary events at a tandem cluster of Arabidopsis thaliana genes resulting in a single-locus genetic incompatibility. PLoS Genet 7:e1002164

    Article  PubMed  CAS  Google Scholar 

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109(6):1105–1114

    Article  PubMed  CAS  Google Scholar 

  • Song QJ, Shi JR, Singh S, Fickus EW, Costa JM, Lewis J, Gill BS, Ward R, Cregan PB (2005) Development and mapping of microsatellite (SSR) markers in wheat. Theor Appl Genet 110(3):550–560

    Article  PubMed  CAS  Google Scholar 

  • Sugie A, Murai K, Takumi S (2007) Alteration of respiration capacity and transcript accumulation level of alternative oxidase genes in necrosis lines of common wheat. Genes Genet Syst 82(3):231–239

    Article  PubMed  CAS  Google Scholar 

  • Tsunewaki K (1970) Necrosis and chlorosis genes in common wheat and its ancestral species. Seiken Ziho 22:67–75

    Google Scholar 

  • Wang Y, Wu WH (2010) Plant sensing and signaling in response to K+-deficiency. Mol Plant 3:280–287

    Article  PubMed  CAS  Google Scholar 

  • Yang YF, Furuta Y, Nagata S, Watanabe N (1999) Tetra Chinese Spring with AABB genomes extracted from the hexaploid common wheat (Triticum aestivum), Chinese spring. Genes Genet Syst 74:67–70

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Drs. Harold Bockelman, Bikram S. Gill, Karl Glover, Kim Kidwell and Steven S. Xu for providing seeds, Dr. Justin Faris and two anonymous reviewers for critical reading of this manuscript, and Mr. Wenjie Wei for technical assistance. This project is supported by South Dakota Agricultural Experiment Station (Brookings, SD) and South Dakota Wheat Commission (Pierre, SD).

Author information

Authors and Affiliations

  1. Department of Biology and Microbiology, South Dakota State University, 252 North Plain Biostress Laboratory, Brookings, SD, 57007, USA

    Wanlong Li, Huilan Zhu, Ghana S. Challa & Zhengzhi Zhang

  2. Department of Plant Science, South Dakota State University, 247 North Plain Biostress Laboratory, Brookings, SD, 57007, USA

    Wanlong Li

Authors
  1. Wanlong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huilan Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ghana S. Challa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhengzhi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wanlong Li.

Additional information

Communicated by F. Hochholdinger.

G. S. Challa and Z. Zhang contributed equally to this research.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, W., Zhu, H., Challa, G.S. et al. A non-additive interaction in a single locus causes a very short root phenotype in wheat. Theor Appl Genet 126, 1189–1200 (2013). https://doi.org/10.1007/s00122-013-2046-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-013-2046-4

Keywords

Search

Navigation