Skip to main content
Log in

Characterization on a Novel Rolled Leaves and Short Petioles Soybean Mutant Based on Seq-BSA and RNA-seq Analysis

  • Research Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

A soybean (Glycine max (Linn.) Merr.) mutant displaying rolled leaves and short petioles was identified as being caused by multiple sites, named rlsp1. Compared to wild-type (WT), the phloem structure of petioles in rlsp1 was not obvious, while the thickness of leaves was significantly greater but the arrangement of leaves cells was relatively looser. Sequencing-based bulked segregant analysis (Seq-BSA) identified 10 candidate regions on chromosomes 3, 6, 8, 13, and 17 with total 6.47 Mb, containing 790 genes. 7946 and 5402 differentially expressed genes (DEGs) were also identified in leaves and petioles, respectively, by RNA-sequencing (RNA-seq). Glyma.03G128600 as orthologs of Arabidopsis BOP (BLADE ON PETIOLES) gene may be the key candidate gene causing the variation of rlsp1. The abnormal development of petiole phloem structure, inhibition of auxin signal transduction pathway, promotion of microtubule-related pathways, and repressed of carbohydrate processes were also closely associated with the formation of rlsp1. These results were further validated by the changes of phytohormones, sucrose, Ca2+, and chlorophyll. The candidate genes found in this study enrich the understanding of the molecular basis for the formation of rolled leaves and short petioles in soybean.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Yoshida K, Mitsuoka C, Tamiru M (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178

    Article  CAS  PubMed  Google Scholar 

  • Ambadipudi R, Georges E (2017) Sequences in linker-1 domain of the multidrug resistance associated protein (MRP1 or ABCC1) bind to tubulin and their binding is modulated by phosphorylation. Biochem Bioph Res Co 482:1001–1006

    Article  CAS  Google Scholar 

  • Anders S, Pyl PT, Huber W (2015) HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169

    Article  CAS  PubMed  Google Scholar 

  • Arase S, Hase Y, Abe J, Kasai M, Yamada T, Kitamura K, Narumi L, Tanaka A, Kanazawa A (2011) Optimization of ion-beam irradiation for mutagenesis in soybean: effects on plant growth and production of visibly altered mutants. Plant Biotechnol-Nar 28:323–329

    Article  CAS  Google Scholar 

  • Babb VM, Haigler CH (2001) Sucrose phosphate synthase activity rises in correlation with high-rate cellulose synthesis in three heterotrophic systems. Plant Physiol 127:1234–1242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blume YB, Krasylenko YA, Yemets AI (2012) Effects of phytohormones on the cytoskeleton of the plant cell. Russ J Plant Physl 59:515–529

    Article  CAS  Google Scholar 

  • Bowma JL, Baum EY, SF, (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18:134–141

    Article  Google Scholar 

  • Bowman JL, Eshed Y, Baum SF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18:134–141

    Article  CAS  PubMed  Google Scholar 

  • Braam J (2005) In touch: plant responses to mechanical stimuli. New Phytol 165:373–389

    Article  PubMed  Google Scholar 

  • Braun N, Wyrzykowska J, Muller P, David K, Couch D, Perrot-Rechenmann C, Fleming AJ (2008) Conditional repression of AUXIN BINDING PROTEIN1 reveals that it coordinates cell division and cell expansion during postembryonic shoot development in Arabidopsis and Tobacco. Plant Cell 20:2746–2762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byrne ME (2005) Networks in leaf development. Curr Opin Plant Biol 8:59–66

    Article  PubMed  Google Scholar 

  • Chen ZL, Liu LN, Liu L, Liu XL (2007) The Role of Microtubules During Cotton Fibers Elongation. Journal of Capital Normal University (natural science edition) 28:50–54

    CAS  Google Scholar 

  • Chin D, Means AR (2000) Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10:322–328

    Article  CAS  PubMed  Google Scholar 

  • Cingolani P, Platts A, Wang LL, Coon M, Luan NT, Wang, et al (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SNP Eff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6:80–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Couzigou JM, Zhukov V, Mondy S, Ghada AEH, Cosson V, Ellis THN, Ambrose M, Wen J, Tadege M, Tikhonovich I (2012) NODULT ROOT and COCHLEATA maintain nodule development and are legume orthologs of Arabidopsis BLADE-ON-PETIOLE genes. Plant Cell 24:4498–4510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cyr RJ (1991) Calcium/calmodulin affects microtubule stability in lysed protoplasts. J Cell Sci 100:311–317

    Article  CAS  Google Scholar 

  • Davis PJ (2005) Plant hormones: biosynthesis, signal transduction, action. Publish Springer, New York

    Google Scholar 

  • Delmer DP, Haigler CH (2002) The regulation of metabolic flux to cellulose, a major sink for carbon in plants. Metab Eng 4:22–28

    Article  CAS  PubMed  Google Scholar 

  • Duncan WG (1971) Leaf angles, leaf area, and canopy photosynthesis1. Crop Sci 11:482–484

    Article  Google Scholar 

  • Einhellig FA, Rasmussen JA (1979) Effects of three phenolic acids on chlorophyll content and growth of soybean and grain sorghum seedlings. J Chem Ecol 5:815–824

    Article  CAS  Google Scholar 

  • Endow SA, Higuchi H (2000) A mutant of the motor protein kinesin that moves in both directions on microtubules. Nature 406:913–916

    Article  CAS  PubMed  Google Scholar 

  • Esteve-Bruna D, Pérez-Pérez JM, Ponce MR, Micol JL (2013) Incurvata13, a novel allele of AUXIN RESISTANT6, reveals a specific role for auxin and the SCF complex in Arabidopsis embryogenesis, vascular specification, and leaf flatness. J Plant Physiol 161:1303–1320

    Article  CAS  Google Scholar 

  • Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L) Merrill. Crop Sci 11:929–931

    Article  Google Scholar 

  • Friml J, Wisniewska J, Benkova E, Palme KMK (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809

    Article  PubMed  Google Scholar 

  • Gibson SI (2000) Arabidopsis Genome: A Milestone in Plant Biology || Plant Sugar-Response Pathways. Part of a Complex Regulatory Web. Plant Physiol 124:1532–1539.

  • Giddings TH, Staehelin LA (1991) Microtubule-mediated control of microfibril deposition: a re-examination of the hypothesis. In the Cytoskeletal Basis of Plant Growth and Form, London, pp 85–99

    Google Scholar 

  • Ha CM (2004) BLADE-ON-PETIOLE1 Encodes a BTB/POZ Domain Protein Required for Leaf Morphogenesis in Arabidopsis thaliana. Plant Cell Physiol 45:1361–1370

    Article  CAS  PubMed  Google Scholar 

  • Ha CM, Jun JH, Fletcher JC (2010) Control of Arabidopsis leaf morphogenesis through regulation of the YABBY and KNOX families of transcription factors. Genetics 186:197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hase Y, Nozawa S, Narumi I, Oono Y (2017) Effects of ion beam irradiation on size of mutant sector and genetic damage in Arabidopsis. Nucl Instrum Methods Phys Res Sect B 391:14–19

    Article  CAS  Google Scholar 

  • He Z (1993) Guidance to Experiment on Chemical Control in Crop Plants. Beijing Agricultural University Publishers, Beijing, pp 60–68

    Google Scholar 

  • Himmelspach R, Williamson RE, Wasteneys GO (2003) Cellulose microfibril alignment recovers from DCB-induced disruption despite microtubule disorganization. Plant J 36:5–575

    Article  CAS  Google Scholar 

  • Izhaki A, Bowman JL (2007) KANADI and class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell 19:5–508

    Article  CAS  Google Scholar 

  • Koch KE, Zeng Y, Yong WT, Avigne W (2000) Multiple paths of sugar-sensing and a sugar/oxygen overlap for genes of sucrose and ethanol metabolism. J Exp Bot 51:417–427

    Article  CAS  PubMed  Google Scholar 

  • Lee EA, Jo HY, Han IS (2005) Auxin Activates Promoter of a Soybean β-tubulin, tubB1 Gene Korean J Genetic 27:383–388.

  • Lee J, Park JJ, Kim SL, Yim J, An J (2007) Mutations in the rice Liguleless gene result in a complete loss of the auricle, ligule, and laminar joint. Plant Mol Biol 65:487–499

    Article  CAS  PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu HL, Xu YY, Xu ZH, Chong K (2007) A rice YABBY gene, OsYABBY4, preferentially expresses in developing vascular tissue. Dev Genes Evol 217:629–637

    Article  CAS  PubMed  Google Scholar 

  • Luo SW, Zhou LB, L WJ, Du Y, Yu LX, Feng H, Mu JH, Chen YZ (2016) Mutagenic effects of carbon ion beam irradiations on dry lotus japonicus seeds. Nucl Instrum Meth B 383:123–128

    Article  CAS  Google Scholar 

  • Machida C, Nakagawa A, Kojima S, Takahashi H, Machida Y (2015) The complex of asymmetric leaves (as) proteins plays a central role in antagonistic interactions of genes for leaf polarity specification in Arabidopsis. Wires Dev Biol 4:655

    Article  CAS  Google Scholar 

  • Matsumoto N, Okada K (2001) A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Gene Dev 15:3355–3364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melkov A, Abdu U (2017) Regulation of long-distance transport of mitochondria along microtubules. Cell Mol Life Sci 75:163

    Article  PubMed  CAS  Google Scholar 

  • Moreno MA, Harper LC, Krueger RW, Dellaporta SL, Freeling M (1997) Liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize organogenesis. Genes Dev 11:616–628

    Article  CAS  PubMed  Google Scholar 

  • Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, Bielach A et al (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–1140

    Article  CAS  PubMed  Google Scholar 

  • Nardmann J, Ji J, Werr W, Scanlon MJ (2004) The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131:2827–2839

    Article  CAS  PubMed  Google Scholar 

  • Norberg M (2005) The blade on petiole genes act redundantly to control the growth and development of lateral organs. Development 132:2203–2213

    Article  CAS  PubMed  Google Scholar 

  • Paffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:9

    Google Scholar 

  • Palni LMS, Burch L, Horgan R (1988) The effect of auxin concentration on cytokinin stability and metabolism. Planta 174:231–234

    Article  CAS  PubMed  Google Scholar 

  • Qin GJ, Gu HY, Zhao YD, Ma ZQ, Shi GL, Yang Y, Pichersky E, Chen HD, Liu Mh, Chen ZH (2005) An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development. Plant Cell 17:2693–2704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with Stresses: Roles of Calcium- and Calcium/ Calmodulin-Regulated Gene Expression. Plant Cell 23:2010–2032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260

    Article  CAS  PubMed  Google Scholar 

  • Rischitor PE, KonzackS FR (2004) The Kip3-like kinesin KipB moves along microtubules and determines spindle position during synchronized mitoses in Aspergillus nidulans hyphae. Eukaryot Cell 3:632–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H, Inzé D, Murphy AS, Overvoorde PJ, Gray WM (2012) The saur19 subfamily of small auxin up RNA genes promote cell expansion. Plant J 70:978–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645

    Article  CAS  PubMed  Google Scholar 

  • Tanaka A, Shikazono N, Hase Y (2010) Studies on biological effects of ion beams on lethality, molecular nature of mutation, mutation rate, and spectrum of mutation phenotype for mutation breeding in higher plants. J Radiat Res 51:223–233

    Article  CAS  PubMed  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tu BJ, Liu CK, Tian BW, Zhang QY, Liu XB, Herbert SJ (2017) Reduced abscisic acid content is responsible for enhanced sucrose accumulation by potassium nutrition in vegetable soybean seeds. J Plant Res 130:551–558

    Article  CAS  PubMed  Google Scholar 

  • Turgeon R, Wolf S (2009) Phloem Transport: Cellular Pathways and Molecular Trafficking. Annu Rev Plan Biol 60:207–221

    Article  CAS  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/lAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136: 1005–1016. Weijschede JE, Antonise K, Caluwe HD, Kroon HD, Huber H (2008) Effects of cell number and cell size on petiole length variation in a stoloniferous herb. Am J Bot 95:41–49

    Google Scholar 

  • Weiler EW, Jourdan PS, Conrad W (1981) Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immuno-assay. Planta 153:561–571

    Article  CAS  PubMed  Google Scholar 

  • Xie B, Dengn Y, Kanaoka MM, Okada K, Hong Z (2012) Expression of Arabidopsis callose synthase 5 results in callose accumulation and cell wall permeability alteration. Plant Sci 183:1–8

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Yang L, Huang H (2007) Transcriptional, post-transcriptional and post-translational regulations of gene expression during leaf polarity formation. Cell Res 17:512–519

    Article  CAS  PubMed  Google Scholar 

  • Xue GQ, Liu Q, Han YQ, Wei HG, Dong T (2006) Determination of thirteen metal elements in the plant foeniculum vulgare mill. by flame atomic absorption spectrophotometry. Spectroscopy and Spectral Analysis 26:1935–1938

    CAS  PubMed  Google Scholar 

  • Yamakawa H, Mitsuhara I, Ito N, Seo S, Kamada H, Ohashi Y (2001) Transcriptionally and post-transcriptionally regulated response of 13 calmodulin genes to tobacco mosaic virus-induced cell death and wounding in tobacco plant. Eur J Biochem 268:3619–3929

    Article  Google Scholar 

  • Yan S, Yan CJ, Gu MH (2008) Molecular mechanism of leaf development Hereditas (Beijing) 30:1127–1135

    Article  CAS  Google Scholar 

  • Yang G, Luo W, Zhang J, Yan X, Guo T (2019) Genome-wide comparisons of mutations induced by carbon-ion beam and gamma-rays irradiation in rice via resequencing multiple mutants. Fron Plant Sci: 10.

  • Yoshida S, Mandel T, Kuhlemeier C (2011) Stem cell activation by light guides plant organogenesis. Gen Dev 25:1439–1450

    Article  CAS  Google Scholar 

  • Zeng HQ, Zhang YX, Zhang XJ, Pi E, Zhu Y (2017) Analysis of EF-Hand Proteins in Soybean Genome Suggests Their Potential Roles in Environmental and Nutritional Stress Signaling. Front Plant Sci 8:877

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang GH, Xu Q, Zhu XD, Xue HW (2009) SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell 21:719–735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao J, Wang J, An L, Doerge W, Chen J, Grau CR, Meng JL, Osborn TG (2007) Analysis of gene expression profiles in response to Sclerotinia sclerotiorum in Brassica Napus. Planta 227:13–24

    Article  CAS  PubMed  Google Scholar 

  • Zhao PM, Wang LL, Han LB, Wang J, Yao J, Wang HY (2010) Proteomic identification of differentially expressed proteins in the Ligon lintless mutant of upland cotton (Gossypium hirsutum L.). J Proteome Res 9:1076–1087

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was partially funded by Major Program of National Science and Technology of China (2016YFD0102105) and Regional Key Project of Science and Technology Service Network from the Chinese Academy of Sciences (KFJ-STS-QYZX-126).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Qiuying Zhang.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 99 KB)

Supplementary file2 (XLSX 67 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Liu, C., Tu, B. et al. Characterization on a Novel Rolled Leaves and Short Petioles Soybean Mutant Based on Seq-BSA and RNA-seq Analysis. J. Plant Biol. 65, 261–277 (2022). https://doi.org/10.1007/s12374-020-09295-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-020-09295-x

Keywords

Navigation