Genetic localization of the SPC gene controlling pod coiling direction in Medicago truncatula

Abstract

Background

Handedness in plants introduced by helical growth of organs is frequently observed, and it has fascinated plant scientists for decades. However, the genetic control of natural handedness has not been revealed. In the model legume Medicago truncatula, pods can be coiled in a clockwise or anti-clockwise manner, providing a model for genetic analysis of plant handedness.

Objective

We aimed to localize the Sense of Pod Coiling (SPC) gene controlling pod coiling direction in M. truncatula.

Methods

Linkage analysis was used with a biparental population for fine mapping of the SPC gene. The genome sequence of M. truncatula Mt4.0 was used for marker identification and physical mapping. Single nucleotide polymorphisms (SNPs) between the parental lines were converted to CAPS (cleaved amplified polymorphic sequences) markers. Genetic map was constructed using the software JoinMap version 3.0. Gene predication and annotation provided by the M. truncatula genome database (http://www.medicagogenome.org) was confirmed with the programs of FGENESH and Pfam 32.0, respectively. Quantitative reverse transcription PCR (qRT-PCR) was used to analyze the relative expression levels of candidate genes.

Results

The genetic analysis indicated that the anti-clockwise coiling is dominant to clockwise and is controlled by the single gene, SPC. The SPC gene was delimited to a 250 kb-region on Chromosome 7. Total of 15 protein-coding genes were identified in the SPC locus through gene annotation and sequence analysis. Of those, two genes, potentially encoding a receptor-like kinase and a vacuolar cation/proton exchanger respectively, were selected as candidates for the SPC gene.

Conclusions

The result presented here lay a foundation for gene cloning of SPC, which will help us to understand the molecular mechanisms underlying helical growth in plant organs.

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References

  1. Bassil E, Coku A, Blumwald E (2012) Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H + antiporters in plant growth and development. J Exp Bot 63(16):5727–5740. https://doi.org/10.1093/jxb/ers250

    CAS  Article  PubMed  Google Scholar 

  2. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL, Studholme DJ, Yeats C, Eddy SR (2004) The Pfam protein families database. Nucleic Acids Res 32(Database issue):D138–D141. https://doi.org/10.1093/nar/gkh121

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Burk DH, Ye ZH (2002) Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule-severing protein. Plant Cell 14(9):2145–2160. https://doi.org/10.1105/tpc.003947

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Buschmann H, Borchers A (2020) Handedness in plant cell expansion: a mutant perspective on helical growth. New Phytol 225(1):53–69. https://doi.org/10.1111/nph.16034

    Article  PubMed  Google Scholar 

  5. Chevalier D, Batoux M, Fulton L, Pfister K, Yadav RK, Schellenberg M, Schneitz K (2005) STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proc Natl Acad Sci USA 102(25):9074–9079. https://doi.org/10.1073/pnas.0503526102

    CAS  Article  PubMed  Google Scholar 

  6. Dong WB, Li DL, Qiu NW, Song YG (2018) The functions of plant cation/proton antiporters. Biol Plant 62(3):421–427. https://doi.org/10.1007/s10535-018-0790-7

    CAS  Article  Google Scholar 

  7. Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, Liu MC, Maman J, Steinhorst L, Schmitz-Thom I, Yvon R, Kudla J, Wu HM, Cheung AY, Dinneny JR (2018) The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca(2+) signaling. Curr Biol 28(5):666–675 e665. https://doi.org/10.1016/j.cub.2018.01.023

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Fourquin C, del Cerro C, Victoria FC, Vialette-Guiraud A, de Oliveira AC, Ferrandiz C (2013) A change in SHATTERPROOF protein lies at the origin of a fruit morphological novelty and a new strategy for seed dispersal in Medicago genus. Plant Physiol 162(2):907–917. https://doi.org/10.1104/pp.113.217570

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T (2000) The SPIRAL genes are required for directional control of cell elongation in Aarabidopsis thaliana. Development 127(20):4443–4453

    CAS  PubMed  Google Scholar 

  10. Hashimoto T (2002) Molecular genetic analysis of left-right handedness in plants. Philos Trans R Soc Lond Ser B Biol Sci 357:799–808. https://doi.org/10.1098/rstb.2002.1088

    CAS  Article  Google Scholar 

  11. He Y, Zhou J, Shan L, Meng X (2018) Plant cell surface receptor-mediated signaling - a common theme amid diversity. J Cell Sci 131:2. https://doi.org/10.1242/jcs.209353

    CAS  Article  Google Scholar 

  12. Ji H, Pardo JM, Batelli G, Van Oosten MJ, Bressan RA, Li X (2013) The Salt Overly Sensitive (SOS) pathway: established and emerging roles. Mol Plant 6(2):275–286. https://doi.org/10.1093/mp/sst017

    CAS  Article  PubMed  Google Scholar 

  13. Kern VD, Schwuchow JM, Reed DW, Nadeau JA, Lucas J, Skripnikov A, Sack FD (2005) Gravitropic moss cells default to spiral growth on the clinostat and in microgravity during spaceflight. Planta 221(1):149–157. https://doi.org/10.1007/s00425-004-1467-3

    CAS  Article  PubMed  Google Scholar 

  14. Lesins KA, Lesins I (1979) Genus Medicago: (Leguminosae): a taxogenetic study. W. Junk, Boston. https://doi.org/10.1007/978-94-009-9634-2

    Google Scholar 

  15. Li D, Bao Y, Wu X, Jack A, Yang S (2014) The use of CAPS and dCAPS markers in marker-assisted selection for tobacco breeding. In: Shavrukov Y (ed) Cleaved Amplified Polymorphic Sequences (CAPS) markers in plant biology. Nova Science Publishers, Hauppauge, pp 137–150

    Google Scholar 

  16. Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404(6779):766–770. https://doi.org/10.1038/35008089

    CAS  Article  PubMed  Google Scholar 

  17. Lilienfeld FA, Kihara H (1956) Dextrality and sinistrality in plants. Proc Acad Jap 32:620–632. https://doi.org/10.1007/s13258-020-00947-3

    CAS  Article  Google Scholar 

  18. Liu H, Wang Q, Yu M, Zhang Y, Wu Y, Zhang H (2008) Transgenic salt-tolerant sugar beet (Beta vulgaris L.) constitutively expressing an Arabidopsis thaliana vacuolar Na/H antiporter gene, AtNHX3, accumulates more soluble sugar but less salt in storage roots. Plant Cell Environ 31(9):1325–1334. https://doi.org/10.1111/j.1365-3040.2008.01838.x

    CAS  Article  PubMed  Google Scholar 

  19. McCubbin T, Bassil E, Zhang S, Blumwald E (2014) Vacuolar Na(+)/H(+) NHX-type antiporters are required for cellular K(+) homeostasis, microtubule organization and directional root growth. Plants (Basel) 3(3):409–426. https://doi.org/10.3390/plants3030409

    CAS  Article  Google Scholar 

  20. Nakajima K, Furutani I, Tachimoto H, Matsubara H, Hashimoto T (2004) SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16(5):1178–1190. https://doi.org/10.1105/tpc.017830

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312(5779):1491–1495. https://doi.org/10.1126/science.1126551

    CAS  Article  PubMed  Google Scholar 

  22. Qiu QS, Barkla BJ, Vera-Estrella R, Zhu JK, Schumaker KS (2003) Na+/H + exchange activity in the plasma membrane of Arabidopsis. Plant Physiol 132(2):1041–1052. https://doi.org/10.1104/pp.102.010421

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Qiu QS, Guo Y, Quintero FJ, Pardo JM, Schumaker KS, Zhu JK (2004) Regulation of vacuolar Na+/H + exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. J Biol Chem 279(1):207–215. https://doi.org/10.1074/jbc.M307982200

    CAS  Article  PubMed  Google Scholar 

  24. Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na + homeostasis. Proc Natl Acad Sci USA 99(13):9061–9066. https://doi.org/10.1073/pnas.132092099

    CAS  Article  PubMed  Google Scholar 

  25. Saffer AM, Carpita NC, Irish VF (2017) Rhamnose-containing cell wall polymers suppress helical plant growth independently of microtubule orientation. Curr Biol 27(15):2248–2259. https://doi.org/10.1016/j.cub.2017.06.032

    CAS  Article  PubMed  Google Scholar 

  26. Sedbrook JC, Kaloriti D (2008) Microtubules, MAPs and plant directional cell expansion. Trends Plant Sci 13(6):303–310. https://doi.org/10.1016/j.tplants.2008.04.002

    CAS  Article  PubMed  Google Scholar 

  27. Serrano-Cartagena J, Robles P, Ponce MR, Micol JL (1999) Genetic analysis of leaf form mutants from the Arabidopsis Information Service collection. Mol Gen Genet 261(4–5):725–739. https://doi.org/10.1007/s004380050016

    CAS  Article  PubMed  Google Scholar 

  28. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H + antiporter. Proc Natl Acad Sci USA 97(12):6896–6901. https://doi.org/10.1073/pnas.120170197

    CAS  Article  PubMed  Google Scholar 

  29. Shih HW, Miller ND, Dai C, Spalding EP, Monshausen GB (2014) The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Curr Biol 24(16):1887–1892. https://doi.org/10.1016/j.cub.2014.06.064

    CAS  Article  PubMed  Google Scholar 

  30. Shoji T, Narita NN, Hayashi K, Asada J, Hamada T, Sonobe S, Nakajima K, Hashimoto T (2004) Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis. Plant Physiol 136(4):3933–3944. https://doi.org/10.1104/pp.104.051748

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Shoji T, Suzuki K, Abe T, Kaneko Y, Shi H, Zhu JK, Rus A, Hasegawa PM, Hashimoto T (2006) Salt stress affects cortical microtubule organization and helical growth in Arabidopsis. Plant Cell Physiol 47(8):1158–1168. https://doi.org/10.1093/pcp/pcj090

    CAS  Article  PubMed  Google Scholar 

  32. Small E, Brookes B (1984) Coiling of alfalfa pods in relation to resistance against seed chalcids: additional observations. Can J Plant Sci 64:659–665

    Article  Google Scholar 

  33. Smyth DR (2016) Helical growth in plant organs: mechanisms and significance. Development 143(18):3272–3282. https://doi.org/10.1242/dev.134064

    CAS  Article  PubMed  Google Scholar 

  34. Solovyev V, Salamov A (1997) The Gene-Finder computer tools for analysis of human and model organisms genome sequences. Proc Int Conf Intell Syst Mol Biol 5:294–302

    CAS  PubMed  Google Scholar 

  35. Sunohara H, Kawai T, Shimizu-Sato S, Sato Y, Sato K, Kitano H (2009) A dominant mutation of TWISTED DWARF 1 encoding an alpha-tubulin protein causes severe dwarfism and right helical growth in rice. Genes Genet Syst 84(3):209–218. https://doi.org/10.1266/ggs.84.209

    CAS  Article  PubMed  Google Scholar 

  36. Tang H, Krishnakumar V, Bidwell S, Rosen B, Chan A, Zhou S, Gentzbittel L, Childs KL, Yandell M, Gundlach H, Mayer KF, Schwartz DC, Town CD (2014) An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genom 15:312. https://doi.org/10.1186/1471-2164-15-312

    CAS  Article  Google Scholar 

  37. Thitamadee S, Tuchihara K, Hashimoto T (2002) Microtubule basis for left-handed helical growth in Arabidopsis. Nature 417(6885):193–196. https://doi.org/10.1038/417193a

    CAS  Article  PubMed  Google Scholar 

  38. Thoquet P, Gherardi M, Journet EP, Kereszt A, Ane JM, Prosperi JM, Huguet T (2002) The molecular genetic linkage map of the model legume Medicago truncatula: an essential tool for comparative legume genomics and the isolation of agronomically important genes. BMC Plant Biol 2:1

    Article  Google Scholar 

  39. Van der Does D, Boutrot F, Engelsdorf T, Rhodes J, McKenna JF, Vernhettes S, Koevoets I, Tintor N, Veerabagu M, Miedes E, Segonzac C, Roux M, Breda AS, Hardtke CS, Molina A, Rep M, Testerink C, Mouille G, Hofte H, Hamann T, Zipfel C (2017) The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses. PLoS Genet 13(6):e1006832. https://doi.org/10.1371/journal.pgen.1006832

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Wang HL, Grusak MA (2005) Structure and development of Medicago truncatula pod wall and seed coat. Ann Bot 95(5):737–747. https://doi.org/10.1093/aob/mci080

    Article  PubMed  PubMed Central  Google Scholar 

  41. Wang C, Li J, Yuan M (2007) Salt tolerance requires cortical microtubule reorganization in Arabidopsis. Plant Cell Physiol 48(11):1534–1547. https://doi.org/10.1093/pcp/pcm123

    CAS  Article  PubMed  Google Scholar 

  42. You EM, Liu KF, Huang SW, Chen M, Groumellec ML, Fann SJ, Yu HT (2010) Construction of integrated genetic linkage maps of the tiger shrimp (Penaeus monodon) using microsatellite and AFLP markers. Anim Genet 41(4):365–376. https://doi.org/10.1111/j.1365-2052.2009.02014.x

    CAS  Article  PubMed  Google Scholar 

  43. Young ND, Debelle F, Oldroyd GE, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KF, Gouzy J, Schoof H et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480(7378):520–524. https://doi.org/10.1038/nature10625

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Dr. Hongyan Zhu for sharing the RILs of A17 × A20, which was originally developed by Dr. Thierry Huguet. This work was supported by the College of Agriculture of the University of Kentucky (to S.Y.) and a Grant from KTRDC Summit (to S.Y.).

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Correspondence to Shengming Yang.

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Yu, X., Qin, Q., Wu, X. et al. Genetic localization of the SPC gene controlling pod coiling direction in Medicago truncatula. Genes Genom 42, 735–742 (2020). https://doi.org/10.1007/s13258-020-00947-3

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Keywords

  • Plant handedness
  • M. truncatula
  • Pod coiling
  • SPC
  • Genetic mapping