Skip to main content
SpringerLink
Log in

Systematic Identification, Evolution and Expression Analysis of the SPL Gene Family in Sugarcane (Saccharum spontaneum)

  • Published:
Tropical Plant Biology Aims and scope Submit manuscript

Abstract

Sugarcane is an important sugar and energy crop that is widely grown in tropical and subtropical regions worldwide. SPL genes are a type of plant-specific transcription factor and play key roles in plant growth and development. Here, 17 SPL genes were identified from Saccharum spontaneum. A phylogenetic analysis of 72 SPLs from four species showed that the SPL family was divided into six groups and may have originated from at least two different last common ancestors. Comparative gene structure analysis revealed that the SPL family underwent exon gain or loss during evolution. Synteny analysis indicated that segmental duplication mainly contributed to the expansion of the SPL family in sugarcane. Eleven SsSPLs were predicted to have potential miR156 binding sites. Expression pattern analysis showed that the SsSPL gene family was functionally differentiated, besides, there also may be functional redundancy among paralogous SPL genes. SsSPL genes in clade I may be involved mainly in the development of reproductive organs, while SsSPL genes in clade VI, including SsSPL13, SsSPL1 and SsSPL16, participate predominantly in the development of various tissues during the vegetative growth stage. These results lay a foundation for further functional analysis of SPL in sugarcane.

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
Fig. 9

Similar content being viewed by others

Abbreviations

AP1:

APETALA1

CDD:

Conserved domain database

CDS:

Coding sequences

CRR1:

Copper response regulator 1

DEP1:

Dense and erect panicle1

GA:

Gibberelic acid

GLW7:

Grain length and width 7

GW7:

Grain width 7

IPA1:

Ideal Plant Architecture 1

Ka:

Non-synonymous substitutions rate

Ks:

Synonymous substitutions rate

LCA:

Last common ancestors

LG1:

LIGULELESS1

ML:

Maximum likelihood

MRE:

miRNA responsive element

Mw:

Molecular weight

NLS:

Nuclear localization signal

ORF:

Open reading frame

SBP:

Squamosa promoter binding protein

SPL:

SQUAMOSA-promoter binding protein-like

TGA1:

Teosinte glume architecture1

TPM:

Transcripts per-kilobase million

References

  • Becraft PW, Bongard-Pierce DK, Sylvester AW, Poethig RS, Freeling M (1990) The liguleless-1 gene acts tissue specifically in maize leaf development. Dev Biol 141:220–232

    Article  CAS  PubMed  Google Scholar 

  • Birkenbihl RP, Jach G, Saedler H, Huijser P (2005) Functional dissection of the plant-specific SBP-domain: overlap of the DNA-binding and nuclear localization domains. J Mol Biol 352:585–596

    Article  CAS  PubMed  Google Scholar 

  • Cai C, Guo W, Zhang B (2018) Genome-wide identification and characterization of SPL transcription factor family and their evolution and expression profiling analysis in cotton. Sci Rep 8:762

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cardon GH, Höhmann S, Nettesheim K, Saedler H, Huijser P (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J 12:367–377

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Cheng H, Hao M, Wang W, Mei D, Tong C, Wang H, Liu J, Fu L, Hu Q (2016) Genomic identification, characterization and differential expression analysis of SBP-box gene family in Brassica napus. BMC Plant Biol 16:196

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chuck G, Whipple C, Jackson D, Hake S (2010) The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137:1243–1250

    Article  CAS  PubMed  Google Scholar 

  • Chuck GS, Brown PJ, Meeley R, Hake S (2014) Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation. Proc Natl Acad Sci U S A 111:18775–18780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conant GC, Wolfe KH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9:938–950

    Article  CAS  PubMed  Google Scholar 

  • D’Hont A, Ison D, Alix K, Roux C, Glaszmann JC (1998) Determination of basic chromosome numbers in the genus Saccharum by physical mapping of ribosomal RNA genes. Genome, 221–225

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155-159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eriksson M, Moseley JL, Tottey S, Del Campo JA, Quinn J, Kim Y, Merchant S (2004) Genetic dissection of nutritional copper signaling in chlamydomonas distinguishes regulatory and target genes. Genetics 168:795–807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gandikota M, Birkenbihl RP, Höhmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3’ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49:683–693

    Article  CAS  PubMed  Google Scholar 

  • Guo AY, Zhu QH, Gu X, Ge S, Yang J, Luo J (2008) Genome-wide identification and evolutionary analysis of the plant specific SBP-box transcription factor family. Gene 418:1–8

    Article  CAS  PubMed  Google Scholar 

  • Hoang NV, Furtado A, Botha FC, Simmons BA, Henry RJ (2015) Potential for Genetic Improvement of Sugarcane as a Source of Biomass for Biofuels. Frontiers in Bioengineering and Biotechnology 3:182

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoang TV, Vo KTX, Rahman MM, Choi SH, Jeon JS (2019) Heat stress transcription factor OsSPL7 plays a critical role in reactive oxygen species balance and stress responses in rice. Plant Sci 289:110273

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, He Y, Chen X, Zhang X, Guo Y, Yang S, Huang J, Traw MB (2020) CRISPR-based assessment of genomic structure in the conserved SQUAMOSA promoter-binding-like gene clusters in rice. Plant J 104:1301–1314

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X et al (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544

    Article  CAS  PubMed  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  PubMed  Google Scholar 

  • Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol Gen Genet 250:7–16

    CAS  PubMed  Google Scholar 

  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 70 for Bigger Datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Li C, Lu S (2014) Molecular characterization of the SPL gene family in Populus trichocarpa. BMC Plant Biol 14:131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR et al (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42:1060–1067

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Song Q, Zhang Y, Li Z, Guo J, Chen X, Zhang G (2020) Genome-wide identification, characterization, and expression patterns analysis of the SBP-box gene family in wheat (Triticum aestivum L). Sci Rep 10:17250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Z, Yu H, Xiong G, Wang J, Jiao Y, Liu G, Jing Y, Meng X, Hu X, Qian Q et al (2013) Genome-wide binding analysis of the transcription activator ideal plant architecture1 reveals a complex network regulating rice plant architecture. Plant Cell 25:3743–3759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948–952

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549

    Article  CAS  PubMed  Google Scholar 

  • Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122–128

    Article  CAS  PubMed  Google Scholar 

  • Peng X, Wang Q, Zhao Y, Li X, Ma Q (2019) Comparative genome analysis of the SPL gene family reveals novel evolutionary features in maize. Genet Mol Biol 42:380–394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    Article  CAS  PubMed  Google Scholar 

  • Shao Y, Zhou HZ, Wu Y, Zhang H, Lin J, Jiang X, He Q, Zhu J, Li Y, Yu H et al (2019) OsSPL3, an SBP-domain protein, regulates crown root development in rice. Plant Cell 31:1257–1275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shikata M, Koyama T, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis SBP-box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase. Plant Cell Physiol 50:2133–2145

    Article  CAS  PubMed  Google Scholar 

  • Si L, Chen J, Huang X, Gong H, Luo J, Hou Q, Zhou T, Lu T, Zhu J, Shangguan Y et al (2016) OsSPL13 controls grain size in cultivated rice. Nat Genet 48:447–456

    Article  CAS  PubMed  Google Scholar 

  • Stone JM, Liang X, Nekl ER, Stiers JJ (2005) Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41:744–754

    Article  CAS  PubMed  Google Scholar 

  • Unte US, Sorensen AM, Pesaresi P, Gandikota M, Leister D, Saedler H, Huijser P (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15:1009–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upton G (1992) Fisher’s exact test. J Roy Stat Soc 155(3):395–402

    Article  Google Scholar 

  • Usami T, Horiguchi G, Yano S, Tsukaya H (2009) The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty. Development 136:955–964

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Nussbaum-Wagler T, Li B, Zhao Q, Vigouroux Y, Faller M, Bomblies K, Lukens L, Doebley JF (2005) The origin of the naked grains of maize. Nature 436:714–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Zhou L, Shi H, Chern M, Yu H, Yi H, He M, Yin J, Zhu X, Li Y et al (2018) A single transcription factor promotes both yield and immunity in rice. Science 361:1026–1028

    Article  CAS  PubMed  Google Scholar 

  • Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Li S, Liu Q, Wu K, Zhang J, Wang S, Wang Y, Chen X, Zhang Y, Gao C et al (2015) The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet 47:949–954

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Wu K, Yuan Q, Liu X, Liu Z, Lin X, Zeng R, Zhu H, Dong G, Qian Q et al (2012a) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–954

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H et al (2012b) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547

    Article  CAS  PubMed  Google Scholar 

  • Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142:280–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu G, Guo C, Shan H, Kong H (2012) Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci U S A 109:1187–1192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci U S A 99:7530–7535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA Promoter Binding Protein-Like7 Is a Central Regulator for Copper Homeostasis in Arabidopsis. Plant Cell 21:347–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Nunokawa E et al (2004) A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors. J Mol Biol 337:49–63

    Article  CAS  PubMed  Google Scholar 

  • Yuan H, Qin P, Hu L, Zhan S, Wang S, Gao P, Li J, Jin M, Xu Z, Gao Q et al (2019) OsSPL18 controls grain weight and grain number in rice. J Genet Genomics 46:41–51

    Article  PubMed  Google Scholar 

  • Yue E, Li C, Li Y, Liu Z, Xu JH (2017) MiR529a modulates panicle architecture through regulating SQUAMOSA PROMOTER BINDING-LIKE genes in rice (Oryza sativa). Plant Mol Biol 94:469–480

    Article  CAS  PubMed  Google Scholar 

  • Zeng RF, Zhou JJ, Liu SR, Gan ZM, Zhang JZ, and Hu CG (2019) Genome-wide identification and characterization of SQUAMOSA-Promoter-Binding protein (SBP) genes involved in the flowering development of citrus clementina. Biomolecules 9

  • Zhang J, Zhang X, Tang H, Zhang Q, Hua X, Ma X, Zhu F, Jones T, Zhu X, Bowers J et al (2018) Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat Genet 50:1565–1573

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Hu W, Zhu F, Wang L, Yu Q, Ming R, Zhang J (2016) Structure, phylogeny, allelic haplotypes and expression of sucrose transporter gene families in Saccharum. BMC Genomics 17:88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Schwarz S, Saedler H, Huijser P (2007) SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis. Plant Mol Biol 63:429–439

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We kindly thank the Center for Genomics and Biotechnology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University for providing access to Saccharum data. Thanks to my dear friend Huan Zhang for helping to draw the sugarcane plants in Figure 9.

Funding

This research is financially supported by GDAS’ Project of Science and Technology Development (2019GDASYL-0103028); National Key Research and Development Program of China (2018YFD1000503); Special Project for Research and Development in Key areas of Guangdong Province (2019B020238001); The Guangdong Provincial Team of Technical System Innovation for Sugarcane Sisal Hemp Industry (2019KJ104-04).

Author information

Authors and Affiliations

  1. Guangdong Sugarcane Genetic Improvement Engineering Center, Institute of Bioengineering, Guangdong Academy of Sciences, Guangzhou, 510316, China

    Xiaomin Feng, Nannan Zhang, Xiangbo Zhang, Jiayun Wu, Yonghong Huang & Yongwen Qi

  2. Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, College of Agriculture, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Yongjun Wang & Jisen Zhang

  3. The Seed Union Station of Fujian Province, Fuzhou, 350002, China

    Miaohong Ruan

Authors
  1. Xiaomin Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yongjun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nannan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiangbo Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiayun Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yonghong Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Miaohong Ruan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jisen Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yongwen Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XF, JZ and YQ conceived the study and designed the experiments. XF, YW, NZ, XZ JW, YH and MR carried out the experiments. XF and YW analyzed the data. XF wrote the manuscript. JZ, and YQ revised and improved the manuscript. All authors reviewed and approved this submission.

Corresponding author

Correspondence to Yongwen Qi.

Ethics declarations

Conflicts of Interest

The authors declare no conflict of interest.

Additional information

Communicated by Robert Henry.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Feng, X., Wang, Y., Zhang, N. et al. Systematic Identification, Evolution and Expression Analysis of the SPL Gene Family in Sugarcane (Saccharum spontaneum). Tropical Plant Biol. 14, 313–328 (2021). https://doi.org/10.1007/s12042-021-09293-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12042-021-09293-4

Keywords

Search

Navigation