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.
Similar content being viewed by others
References
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
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
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
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
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
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
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
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
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
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
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
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
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
Lesins KA, Lesins I (1979) Genus Medicago: (Leguminosae): a taxogenetic study. W. Junk, Boston. https://doi.org/10.1007/978-94-009-9634-2
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Smyth DR (2016) Helical growth in plant organs: mechanisms and significance. Development 143(18):3272–3282. https://doi.org/10.1242/dev.134064
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
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
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
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
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
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
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
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
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
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
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.).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13258-020-00947-3