Advertisement

Planta

, Volume 250, Issue 5, pp 1621–1635 | Cite as

Cassava AGPase genes and their encoded proteins are different from those of other plants

  • Ming-You Dong
  • Xian-Wei Fan
  • You-Zhi LiEmail author
Original Article

Abstract

Main conclusion

Cassava AGPase and AGPase genes have some unique characteristics.

Abstract

ADP-glucose pyrophosphorylase (AGPase) is a rate-limiting enzyme for starch synthesis. In this study, cassava AGPase genes (MeAGP) were analyzed based on six cultivars and one wild species. A total of seven MeAGPs was identified, including four encoding AGPase large subunits (MeAGPLs 1, 2, 3 and 4) and three encoding AGPase small subunits (MeAGPSs 1, 2 and 3). The copy number of MeAGPs varied in cassava germplasm materials. There were 14 introns for MeAGPLs 1, 2 and 3, 13 introns for MeAGPL4, and 8 introns for other three MeAGPSs. Multiple conservative amino acid sequence motifs were found in the MeAGPs. There were differences in amino acids at binding sites of substrates and regulators among different MeAGP subunits and between MeAGPs and a potato AGPase small subunit (1YP2:B). MeAGPs were all located in chloroplasts. MeAGP expression was not only associated with gene copy number and types/combinations, regions and levels of the DNA methylation but was also affected by environmental factors with the involvement of various transcription factors in multiple regulation networks and in various cis-elements in the gene promoter regions. The MeAGP activity also changed with environmental conditions and had potential differences among the subunits. Taken together, MeAGPs differ in number from those of Arabidopsis, potato, maize, banana, sweet potato, and tomato.

Keywords

Binding sites Enzymes Evolution Genome Starch Transcriptome Subcellular localization 

Abbreviations

AGP

ADP-glucose pyrophosphorylase

AGPL

AGP large subunit

AGPS

AGP small subunit

Arg7

Cassava cultivar Arg7

AtAGP

Arabidopsis AGPase

BL00/03/24

Bottom leaves sampled before/3 h after/24 h after PEG treatment

DAP

Days after planting

FEL00/03

Fully expanded leaves sampled before/3 h after PEG treatment

FL00/24

Folded leaves sampled before/24 h after PEG treatment

F01

Cassava cultivar Fuxuan 01

GEO

Gene Expression Omnibus

KU50

Cassava cv KU50

MeAGP

Cassava AGPase

NTP

Nucleotidyl transferase protein

9I

Cassava cv 9I

OsAGP

Rice AGPase

PEG

Polyethylene glycol

RT00/03/24

Roots sampled before/3 h after/24 h after PEG treatment

SC124

Cassava cv South China 124

16P

Cassava cv 16P

SRA

RNA-seq read archive

W14

Wild cassava species

Notes

Acknowledgements

This work is supported by the Innovation Project of Guangxi Graduate Education (YCBZ2018020) and the funding (SKLCUSA-a201804) from State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources. We are grateful to Professor Wang Wen-Quan of Chinese Academy of Tropical Agricultural Sciences for providing cassava stem cuttings.

Compliance with ethical standards

Conflict of interest

We state no conflict of interest with others.

Ethical statement

Our work complies with the Ethical Rules applicable to this journal.

Supplementary material

425_2019_3247_MOESM1_ESM.docx (17 kb)
Supplementary material 1 (DOCX 16 kb)
425_2019_3247_MOESM2_ESM.docx (21 kb)
Supplementary material 2 (DOCX 20 kb)
425_2019_3247_MOESM3_ESM.docx (15 kb)
Supplementary material 3 (DOCX 15 kb)
425_2019_3247_MOESM4_ESM.docx (15 kb)
Supplementary material 4 (DOCX 15 kb)
425_2019_3247_MOESM5_ESM.docx (17 kb)
Supplementary material 5 (DOCX 17 kb)
425_2019_3247_MOESM6_ESM.docx (16 kb)
Supplementary material 6 (DOCX 15 kb)
425_2019_3247_MOESM7_ESM.docx (20 kb)
Supplementary material 7 (DOCX 19 kb)
425_2019_3247_MOESM8_ESM.docx (16 kb)
Supplementary material 8 (DOCX 15 kb)
425_2019_3247_MOESM9_ESM.docx (17 kb)
Supplementary material 9 (DOCX 17 kb)
425_2019_3247_MOESM10_ESM.docx (22 kb)
Supplementary material 10 (DOCX 21 kb)
425_2019_3247_MOESM11_ESM.docx (20 kb)
Supplementary material 11 (DOCX 19 kb)

References

  1. Aoki K, Ogata Y, Shibata D (2007) Approaches for extracting practical information from gene co-expression networks in plant biology. Plant Cell Physiol 48:381–390PubMedGoogle Scholar
  2. Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, Grosdidier A, Hernandez C, Ioannidis V, Kuznetsov D, Liechti R, Moretti S, Mostaguir K, Redaschi N, Rossier G, Xenarios I, Stockinger H (2012) ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res 40:W597–W603PubMedPubMedCentralGoogle Scholar
  3. Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME Suite. Nucleic Acids Res 43:W39–W49PubMedPubMedCentralGoogle Scholar
  4. Baralle FE, Giudice J (2017) Alternative splicing as a regulator of development and tissue identity. Nat Rev Mol Cell Biol 18:437–451PubMedGoogle Scholar
  5. Beckles DM, Craig J, Smith AM (2001a) ADP-glucose pyrophosphorylase is located in the plastid in developing tomato fruit. Plant Physiol 126:261–266PubMedPubMedCentralGoogle Scholar
  6. Beckles DM, Smith AM, ap Rees T (2001b) A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs. Plant Physiol 125:818–827PubMedPubMedCentralGoogle Scholar
  7. Burton RA, Johnson PE, Beckles DM, Fincher GB, Jenner HL, Naldrett MJ, Denyer K (2002) Characterization of the genes encoding the cytosolic and plastidial forms of ADP-glucose pyrophosphorylase in wheat endosperm. Plant Physiol 130:1464–1475PubMedPubMedCentralGoogle Scholar
  8. Chen X, Xia J, Xia Z, Zhang H, Zeng C, Lu C, Zhang W, Wang W (2015) Potential functions of microRNAs in starch metabolism and development revealed by miRNA transcriptome profiling of cassava cultivars and their wild progenitor. BMC Plant Biol 15:33PubMedPubMedCentralGoogle Scholar
  9. Chen D, Meng L, Pei F, Zheng Y, Leng J (2017) A review of DNA methylation in depression. J Clin Neurosci 43:39–46PubMedGoogle Scholar
  10. Chen CJ, Xia R, Chen H, He YH (2018) TBtools, a toolkit for biologists integrating various HTS-data handling tools with a user-friendly interface. BioRxiv.  https://doi.org/10.1101/289660 CrossRefGoogle Scholar
  11. Cheng YE, Dong MY, Fan XW, Nong LL, Li YZ (2018) A study on cassava tolerance to and growth responses under salt stress. Environ Exp Bot 155:429–440Google Scholar
  12. Comparot-Moss S, Denyer K (2009) The evolution of the starch biosynthetic pathway in cereals and other grasses. J Exp Bot 60:2481–2492PubMedGoogle Scholar
  13. Crevillen P, Ventriglia T, Pinto F, Orea A, Merida A, Romero JM (2005) Differential pattern of expression and sugar regulation of Arabidopsis thaliana ADP-glucose pyrophosphorylase-encoding genes. J Biol Chem 280:8143–8149PubMedGoogle Scholar
  14. Denyer K, Dunlap F, Thorbjornsen T, Keeling P, Smith AM (1996) The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiol 112:779–785PubMedPubMedCentralGoogle Scholar
  15. Ding Z, Fu L, Yan Y, Tie W, Xia Z, Wang W, Peng M, Hu W, Zhang J (2017) Genome-wide characterization and expression profiling of HD-Zip gene family related to abiotic stress in cassava. PLoS One 12:e0173043PubMedPubMedCentralGoogle Scholar
  16. El-Sharkawy MA (2004) Cassava biology and physiology. Plant Mol Biol 56:481–501PubMedGoogle Scholar
  17. Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39(Web Server issue):W29–W37PubMedPubMedCentralGoogle Scholar
  18. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285PubMedGoogle Scholar
  19. Fu FF, Xue HW (2010) Coexpression analysis identifies Rice Starch Regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154:927–938PubMedPubMedCentralGoogle Scholar
  20. Guo YJ, Luo XL, Wei MG, Liu ZL, Fan WJ, Zhai RN, Zhu YM (2018) RNA sequence analysis of cassava varieties with high-starch content using De Novo assembly. J Plant Growth Regul 37:517–529Google Scholar
  21. Hou L, Zhang Z, Dou S, Zhang Y, Pang X, Li Y (2018) Genome-wide identification, characterization, and expression analysis of the expansin gene family in Chinese jujube (Ziziphus jujuba Mill.). Planta 249:815–829PubMedGoogle Scholar
  22. Hu MZ, Hu WB, Xia ZQ, Zhou XC, Wang WQ (2016a) Validation of reference genes for relative quantitative gene expression studies in cassava (Manihot esculenta Crantz) by using quantitative real-time PCR. Front Plant Sci 7:680PubMedPubMedCentralGoogle Scholar
  23. Hu W, Yang H, Yan Y, Wei Y, Tie W, Ding Z, Zuo J, Peng M, Li K (2016b) Genome-wide characterization and analysis of bZIP transcription factor gene family related to abiotic stress in cassava. Sci Rep 6:22783PubMedPubMedCentralGoogle Scholar
  24. Jin X, Ballicora MA, Preiss J, Geiger JH (2005) Crystal structure of potato tuber ADP-glucose pyrophosphorylase. EMBO J 24:694–704PubMedPubMedCentralGoogle Scholar
  25. Kang GZ, Wang YH, Liu C, Shen BQ, Zheng BB, Feng W, Guo TC (2010) Difference in AGPase subunits could be associated with starch accumulation in grains between two wheat cultivars. Plant Growth Regul 61:61–66Google Scholar
  26. Kavakli IH, Greene TW, Salamone PR, Choi SB, Okita TW (2001) Investigation of subunit function in ADP-glucose pyrophosphorylase. Biochem Biophys Res Commun 281:783–787PubMedGoogle Scholar
  27. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefGoogle Scholar
  28. Lee SK, Hwang SK, Han M, Eom JS, Kang HG, Han Y, Choi SB, Cho MH, Bhoo SH, An G, Hahn TR, Okita TW, Jeon JS (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 65:531–546PubMedGoogle Scholar
  29. Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327PubMedPubMedCentralGoogle Scholar
  30. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323Google Scholar
  31. Li X, Zhu J, Hu F, Ge S, Ye M, Xiang H, Zhang G, Zheng X, Zhang H, Zhang S, Li Q, Luo R, Yu C, Yu J, Sun J, Zou X, Cao X, Xie X, Wang J, Wang W (2012) Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genom 13:300Google Scholar
  32. Li MY, Liu EP, Xia QY, Guo YL, Yi XP, Guo AP (2016a) Establishment of qualitative polymerase chain reaction (PCR) and quantitative PCR methods for endogenous reference gene LAM2 in transgenic cassava. Mol Plant Breed 14:153–161 (in Chinese but with English abstract) Google Scholar
  33. Li YZ, Zhao JY, Wu SM, Fan XW, Luo XL, Chen BS (2016b) Characters related to higher starch accumulation in cassava storage roots. Sci Rep 6:19823PubMedPubMedCentralGoogle Scholar
  34. Lu FH, Park YJ (2012) Sequence variations in OsAGPase significantly associated with amylose content and viscosity properties in rice (Oryza sativa L.). Genet Res (Camb) 94:179–189Google Scholar
  35. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(D1):D200–D203PubMedGoogle Scholar
  36. Miao H, Sun P, Liu Q, Liu J, Xu B, Jin Z (2017) The AGPase family proteins in banana: genome-wide identification, phylogeny, and expression analyses reveal their involvement in the development, ripening, and abiotic/biotic stress responses. Int J Mol Sci 18:1581PubMedCentralGoogle Scholar
  37. Mitchell AL, Attwood TK, Babbitt PC, Blum M, Bork P, Bridge A, Brown SD et al (2019) InterPro in 2019: improving coverage, classification and access to protein sequence annotations. Nucleic Acids Res 47(D1):D351–D360PubMedPubMedCentralGoogle Scholar
  38. Okita TW, Nakata PA, Anderson JM, Sowokinos J, Morell M, Preiss J (1990) The subunit structure of potato tuber ADP glucose pyrophosphorylase. Plant Physiol 93:785–790PubMedPubMedCentralGoogle Scholar
  39. Petreikov M, Shen S, Yeselson Y, Levin I, Bar M, Schaffer AA (2006) Temporally extended gene expression of the ADP-Glc pyrophosphorylase large subunit (AgpL1) leads to increased enzyme activity in developing tomato fruit. Planta 224:1465–1479PubMedGoogle Scholar
  40. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45PubMedPubMedCentralGoogle Scholar
  41. Preiss J, Danner S, Summers PS, Morell M, Barton CR, Yang L, Nieder M (1990) Molecular characterization of the Brittle-2 gene effect on maize endosperm ADPglucose pyrophosphorylase subunits. Plant Physiol 92:881–885PubMedPubMedCentralGoogle Scholar
  42. Qu J, Xu S, Zhang Z, Chen G, Zhong Y, Liu L, Zhang R, Xue J, Guo D (2018) Evolutionary, structural and expression analysis of core genes involved in starch synthesis. Sci Rep 8:12736PubMedPubMedCentralGoogle Scholar
  43. Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42(Web Server issue):W320–W324PubMedPubMedCentralGoogle Scholar
  44. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140PubMedPubMedCentralGoogle Scholar
  45. Rösti S, Denyer K (2007) Two paralogous genes encoding small Subunits of ADP-glucose pyrophosphorylase in maize, Bt2 and L2, replace the single alternatively spliced gene found in other cereal species. J Mol Evol 65:316–327PubMedGoogle Scholar
  46. Rösti S, Fahy B, Denyer K (2007) A mutant of rice lacking the leaf large subunit of ADP-glucose pyrophosphorylase has drastically reduced leaf starch content but grows normally. Funct Plant Biol 34:480–489Google Scholar
  47. Saripalli G, Gupta PK (2015) AGPase: its role in crop productivity with emphasis on heat tolerance in cereals. Theor Appl Genet 128:1893–1916PubMedGoogle Scholar
  48. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504PubMedPubMedCentralGoogle Scholar
  49. Shaul O (2017) How introns enhance gene expression. Int J Biochem Cell Biol 91(PtB):145–155PubMedGoogle Scholar
  50. Smidansky ED, Clancy M, Meyer FD, Lanning SP, Blake NK, Talbert LE, Giroux MJ (2002) Enhanced ADP-glucose pyrophosphorylase activity in wheat endosperm increases seed yield. Proc Natl Acad Sci USA 99:1724–1729PubMedGoogle Scholar
  51. Soliman A, Ayele BT, Daayf F (2014) Biochemical and molecular characterization of barley plastidial ADP-glucose transporter (HvBT1). PLoS One 9:e98524PubMedPubMedCentralGoogle Scholar
  52. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729PubMedPubMedCentralGoogle Scholar
  53. Tang XJ, Peng C, Zhang J, Cai Y, You XM, Kong F, Yan HG, Wang GX, Wang L, Jin J, Chen WW, Chen XG, Ma J, Wang P, Jiang L, Zhang WW, Wan JM (2016) ADP-glucose pyrophosphorylase large subunit 2 is essential for storage substance accumulation and subunit interactions in rice endosperm. Plant Sci 249:70–83PubMedGoogle Scholar
  54. Tappiban P, Smith DR, Triwitayakorn K, Bao J (2019) Recent understanding of starch biosynthesis in cassava for quality improvement: a review. Trends Food Sci Tech 83:167–180Google Scholar
  55. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578PubMedPubMedCentralGoogle Scholar
  56. Tuncel A, Okita TW (2013) Improving starch yield in cereals by over-expression of ADPglucose pyrophosphorylase: expectations and unanticipated outcomes. Plant Sci 211:52–60PubMedGoogle Scholar
  57. Van Harsselaar JK, Lorenz J, Senning M, Sonnewald U, Sonnewald S (2017) Genome-wide analysis of starch metabolism genes in potato (Solanum tuberosum L.). BMC Genom 18:37Google Scholar
  58. Wang W, Feng B, Xiao J, Xia Z, Zhou X, Li P, Zhang W, Wang Y, Møller BL et al (2014) Cassava genome from a wild ancestor to cultivated varieties. Nat Commun 5:5110PubMedPubMedCentralGoogle Scholar
  59. Wang H, Beyene G, Zhai J, Feng S, Fahlgren N, Taylor NJ, Bart R, Carrington JC, Jacobsen SE, Ausin I (2015) CG gene body DNA methylation changes and evolution of duplicated genes in cassava. Proc Natl Acad Sci USA 112:13729–13734PubMedGoogle Scholar
  60. Wei Y, Shi H, Xia Z, Tie W, Ding Z, Yan Y, Wang W, Hu W, Li K (2016) Genome-wide identification and expression analysis of the WRKY gene family in cassava. Front Plant Sci 7:25PubMedPubMedCentralGoogle Scholar
  61. Wiberley-Bradford AE, Busse JS, Jiang J, Bethke PC (2014) Sugar metabolism, chip color, invertase activity, and gene expression during long-term cold storage of potato (Solanum tuberosum) tubers from wild-type and vacuolar invertase silencing lines of Katahdin. BMC Res Notes 7:801PubMedPubMedCentralGoogle Scholar
  62. Wilson MC, Mutka AM, Hummel AW, Berry J, Chauhan RD, Vijayaraghavan A, Taylor NJ, Voytas DF, Chitwood DH, Bart RS (2017) Gene expression atlas for the food security crop cassava. New Phytol 213:1632–1641PubMedPubMedCentralGoogle Scholar
  63. Xia J, Zeng C, Chen Z, Zhang K, Chen X, Zhou Y, Song S, Lu C, Yang R, Yang Z, Zhou J, Peng H, Wang W, Peng M, Zhang W (2014) Endogenous small-noncoding RNAs and their roles in chilling response and stress acclimation in Cassava. BMC Genom 15:634Google Scholar
  64. Xiang H, Zhu J, Chen Q, Dai F, Li X, Li M, Zhang H, Zhang G, Li D, Dong Y, Zhao L, Lin Y, Cheng D, Yu J, Sun J, Zhou X, Ma K, He Y, Zhao Y, Guo S, Ye M, Guo G, Li Y, Li R, Zhang X, Ma L, Kristiansen K, Guo Q, Jiang J, Beck S, Xia Q, Wang W, Wang J (2010) Single base-resolution methylome of the silkworm reveals a sparse epigenomic map. Nat Biotechnol 28:516–520PubMedGoogle Scholar
  65. Xiao X, Zhang J, Li T, Fu X, Satheesh V, Niu Q, Lang Z, Zhu JK, Lei M (2019) A group of SUVH methyl-DNA binding proteins regulate expression of the DNA demethylase ROS1 in Arabidopsis. J Integr Plant Biol 61:110–119PubMedGoogle Scholar
  66. Yin YG, Kobayashi Y, Sanuki A, Kondo S, Fukuda N, Ezura H, Sugaya S, Matsukura C (2010) Salinity induces carbohydrate accumulation and sugar-regulated starch biosynthetic genes in tomato (Solanum lycopersicum L. cv. ‘Micro-Tom’) fruits in an ABA- and osmotic stress-independent manner. J Exp Bot 61:563–574PubMedGoogle Scholar
  67. Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64:643–651Google Scholar
  68. Zemach A, Kim MY, Silva P, Rodrigues JA, Dotson B, Brooks MD, Zilberman D (2010) Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci USA 107:18729–18734PubMedGoogle Scholar
  69. Zeng C, Chen Z, Xia J, Zhang K, Chen X, Zhou Y, Bo W, Song S, Deng D, Guo X, Wang B, Zhou J, Peng H, Wang W, Peng M, Zhang W (2014) Chilling acclimation provides immunity to stress by altering regulatory networks and inducing genes with protective functions in cassava. BMC Plant Biol 14:207PubMedPubMedCentralGoogle Scholar
  70. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201PubMedGoogle Scholar
  71. Zhao P, Liu P, Shao J, Li C, Wang B, Guo X, Yan B, Xia Y, Peng M (2015) Analysis of different strategies adapted by two cassava cultivars in response to drought stress: ensuring survival or continuing growth. J Exp Bot 66:1477–1488PubMedGoogle Scholar
  72. Zhao QQ, Lin RN, Li L, Chen S, He XJ (2019) A methylated-DNA-binding complex required for plant development mediates transcriptional activation of promoter methylated genes. J Integr Plant Biol 61:120–139PubMedGoogle Scholar
  73. Zhou YX, Chen YX, Tao X, Cheng XJ, Wang HY (2016) Isolation and characterization of cDNAs and genomic DNAs encoding ADP-glucose pyrophosphorylase large and small subunits from sweet potato. Mol Genet Genom 291:609–620Google Scholar
  74. Zhu LY, Zhu YR, Dai DJ, Wang X, Jin HC (2018) Epigenetic regulation of alternative splicing. Am J Cancer Res 8:2346–2358PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, College of Life Science and TechnologyGuangxi UniversityNanningChina

Personalised recommendations