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Identification of ACC Synthetase Genes in Saccharum and their Expression Profiles During Plant Growth and in Response to Low-nitrogen Stress

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Abstract

Sugarcane (Saccharum spp.) is economically important in China. Ethylene is an important factor in regulating plant growth and sugar accumulation in sugarcane. 1-Aminocyclopropane-1-carboxylic acid synthase (ACS) is a rate-limiting enzyme in ethylene biosynthesis. However, knowledge of the ACS gene family of Saccharum is limited. In this study, we aimed to identify and analyze ACS genes in the genome of Saccharum. Bioinformatic analyses were performed to identify differences between the ACS sequences of Saccharum and homologous gene sequences of plants. The results showed that there were four ACS genes in the genome of Saccharum, and the phylogenetic tree revealed that the proteins encoded by these genes were similar to ACS isozymes with ACS activity in other plants. Evolutionary analyses suggested that the S. spontaneum ACS gene family may have expanded via segmental duplication events under purifying selection. Expression pattern analyses showed that the Saccharum ACS gene family was differentially expressed. ACS2 and ACS3 may be involved mainly in the development of various tissues during the vegetative growth stage and may be involved in the low-nitrogen response in sugarcane. These results provide relevant information to help determine the functions of the ACS genes in Saccharum, particularly the functions in regulating ethylene stimulation of abiotic stress and sugar productivity.

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Abbreviations

ACS:

1-aminocyclopropane-1-carboxylic acid synthase

LN:

Low-nitrogen

RT-qPCR:

Real-time quantitative polymerase chain reaction

BLAST:

Basic local alignment search tool

HMM:

Hidden Markov Model

SMART:

Simple Modular Architecture Research Tool

MEME:

Multiple Expectation Maximization for Motif Elicitation

pI:

isoelectric point

MW:

Molecular weight

FPKM:

Fragments per kilobase million

References

  • Argueso CT, Hansen M, Kieber JJ (2007) Regulation of ethylene biosynthesis. J Plant Growth Regul 26(2):92–105

    Article  CAS  Google Scholar 

  • Bailey TL, Johnson J, Grant CE et al (2015) The MEME suite. Nucleic Acids Res 43(W1):W39–W49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barry CS, Blume B, Bouzayen M (1996) Differential expression of 1-aminocyclopropane-1-carboxylic acid oxidase genes family of tomato. Plant J 9(6):525–535

    Article  CAS  PubMed  Google Scholar 

  • Capitani G, Hohenester E, Feng L et al (1999) Structure of 1-aminocyclopropane-1-carboxylate synthase, a key enzyme in the biosynthesis of the plant hormone ethylene. J Mol Biol 294(3):745–756

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Chen H, Zhang Y et al (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Cheng J, Khan MA, Qiu WM et al (2012) Diversification of genes encoding granule-bound starch synthase in monocots and dicots is marked by multiple genome-wide duplication events.PLoS One7(1), e30088

  • Dong JG, Yip WK, Yang SF (1991) Monoclonal antibodies against apple 1-aminocyclopropane-l-carboxylate synthase. Plant Cell Physiol 32(1):25–31

    CAS  Google Scholar 

  • D’Hont A, Ison D, Alix K et al (1998) Determination of basic chromosome numbers in the genus Saccharum by physical mapping of ribosomal RNA genes. Genome 41(2):221–225

    Article  Google Scholar 

  • El-Sharkawy I, Kim WS, Jayasankar S et al (2008) Differential regulation of four members of the ACC synthase gene family in plum. J Exp Bot 59(8):2009–2027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng X, Wang Y, Zhang N et al (2021a) Comparative phylogenetic analysis of CBL reveals the gene family evolution and functional divergence in Saccharum spontaneum. BMC Plant Biol 21(1):1–14

    Article  CAS  Google Scholar 

  • Feng X, Wang Y, Zhang N et al (2021b) Systematic identification, evolution and expression analysis of the SPL gene family in sugarcane (Saccharum spontaneum).Tropical Plant Biology1–16

  • Finn RD, Coggill P, Eberhardt RY et al (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44(D1):D279–D285

    Article  CAS  PubMed  Google Scholar 

  • Franco HCJ, Otto R, Faroni CE et al (2011) Nitrogen in sugarcane derived from fertilizer under Brazilian field conditions. Field Crops Research 121(1):29–41

    Article  Google Scholar 

  • Gao Y, Ma J, Zheng JC et al (2019) The elongation factor GmEF4 is involved in the response to drought and salt tolerance in soybean. Int J Mol Sci 20(12):3001

    Article  CAS  PubMed Central  Google Scholar 

  • Gopalasundaram P, Bhaskaran A, Rakkiyappan P (2012) Integrated nutrient management in sugarcane. Sugar Tech 14(1):3–20

    Article  CAS  Google Scholar 

  • Habben JE, Bao X, Bate NJ et al (2014) Transgenic alteration of ethylene biosynthesis increases grain yield in maize under field drought-stress conditions. Plant Biotechnol J 12(6):685–693

    Article  CAS  PubMed  Google Scholar 

  • Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98

  • Hansen M, Chae HS, Kieber JJ (2009) Regulation of ACS protein stability by cytokinin and brassinosteroid. Plant J 57(4):606–614

    Article  CAS  PubMed  Google Scholar 

  • Harada T, Murakoshi Y, Torii Y et al (2011) Analysis of genomic DNA of DcACS1, a 1-aminocyclopropane-1-carboxylate synthase gene, expressed in senescing petals of carnation (Dianthus caryophyllus) and its orthologous genes in D. superbus var. longicalycinus. Plant Cell Rep 30(4):519–527

    Article  CAS  PubMed  Google Scholar 

  • Hoang NV, Furtado A, Botha FC et al (2015) Potential for genetic improvement of sugarcane as a source of biomass for biofuels. Front Bioeng Biotechnol 3:182

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu W, Hua X, Zhang Q et al (2018) New insights into the evolution and functional divergence of the SWEET family in Saccharum based on comparative genomics. BMC Plant Biol 18(1):1–20

    Article  Google Scholar 

  • Huai Q, Xia Y, Chen Y et al (2001) Crystal structures of 1-aminocyclopropane-1-carboxylate (ACC) synthase in complex with aminoethoxyvinylglycine and pyridoxal-5′-phosphate provide new insight into catalytic mechanisms. J Biol Chem 276(41):38210–38216

    Article  CAS  PubMed  Google Scholar 

  • Huang SJ, Chang CL, Wang PH et al (2013) A type III ACC synthase, ACS7, is involved in root gravitropism in Arabidopsis thaliana. J Exp Bot 64(14):4343–4360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jakubowicz M, Sadowski J (2002) 1-Aminocyclopropane-l-carboxylate synthase genes and expression. Acta Physiol Plant 24(4):459–478

    Article  CAS  Google Scholar 

  • Jiao Y, Wickett NJ, Ayyampalayam S et al (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345):97–100

    Article  CAS  PubMed  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8(3):275–282

    Article  CAS  Google Scholar 

  • Kamiyoshihara Y, Iwata M, Fukaya T et al (2010) Turnover of LeACS2, a wound-inducible1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. Plant J 64(1):140–150

    CAS  PubMed  Google Scholar 

  • Krzywinski M, Schein J, Birol I et al (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lee JH, Kim YC, Choi D et al (2018) RNA expression, protein activity, and interactions in the ACC synthase gene family in cucumber (Cucumis sativus L.). Environ Biotechnol 59(1):81–91Horticulture

    CAS  Google Scholar 

  • Letunic I, Doerks T, Bork P (2015) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43(D1):D257–D260

    Article  CAS  PubMed  Google Scholar 

  • Liang X, Abel S, Keller JA et al (1992) The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Proceedings of the National Academy of Sciences 89(22), 11046–11050

  • Liang X, Shen NF, Theologis A (1996) Li+-regulated 1-aminocyclopropane-1-carboxylate synthase gene expression in Arabidopsis thaliana. Plant J 10(6):1027–1036

    Article  CAS  PubMed  Google Scholar 

  • Li P, Ponnala L, Gandotra N et al (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42(12):1060–1067

    Article  CAS  PubMed  Google Scholar 

  • Li T, Tan D, Liu Z et al (2015) Apple MdACS6 regulates ethylene biosynthesis during fruit development involving ethylene-responsive factor. Plant Cell Physiol 56(10):1909–1917

    Article  CAS  PubMed  Google Scholar 

  • Liu CY, Lü RH, Li J et al (2014) Characterization and expression profiles of MaACS and MaACO genes from mulberry (Morus alba L.). J Zhejiang University-Science B 15(7):611–623

    Article  CAS  Google Scholar 

  • Li Y, Feng L, Kirsch JF (1997) Kinetic and spectroscopic investigations of wild-type and mutant forms of apple 1-aminocyclopropane-1-carboxylate synthase. Biochemistry 36(49):15477–15488

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Pirrello J, Chervin C et al (2015) Ethylene control of fruit ripening: revisiting the complex network of transcriptional regulation. Plant Physiol 169(4):2380–2390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16(12):3386–3399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290(5494):1151–1155

    Article  CAS  PubMed  Google Scholar 

  • Ming R, VanBuren R, Wai CM et al (2015) The pineapple genome and the evolution of CAM photosynthesis. Nat Genet 47(12):1435–1442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park C, Lee HY, Yoon GM (2021) The regulation of ACC synthase protein turnover: A rapid route for modulating plant development and stress responses. Curr Opin Plant Biol 63:102046

    Article  CAS  PubMed  Google Scholar 

  • Peng HP, Lin TY, Wang NN et al (2005) Differential expression of genes encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis during hypoxia. Plant Mol Biol 58(1):15–25

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues-Pousada RA, De Rycke R, Dedonder A et al (1993) The Arabidopsis 1-aminocyclopropane-1-carboxylate synthase gene 1 is expressed during early development. Plant Cell 5(8):897–911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato T, Theologis A (1989) Cloning the mRNA encoding 1-aminocyclopropane-1-carboxylate synthase, the key enzyme for ethylene biosynthesis in plants. Proc. Natl. Acad. Sci. USA 86(17), 6621–6625

  • Suman A, Kimbeng CA, Edmé SJ et al (2008) Sequence-related amplified polymorphism (SRAP) markers for assessing genetic relationships and diversity in sugarcane germplasm collections. Plant Genetic Resources 6(3):222–231

    Article  Google Scholar 

  • Tarun AS, Lee JS, Theologis A (1998) Random mutagenesis of 1-aminocyclopropane-1-carboxylate synthase: a key enzyme in ethylene biosynthesis. Proc. Natl. Acad. Sci. USA 95(17), 9796–9801

  • Tatsuki M, Mori H (2001) Phosphorylation of tomato 1-aminocyclopropane-1-carboxylic acid synthase, LE-ACS2, at the C-terminal region. J Biol Chem 276(30):28051–28057

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Van de Poel B, Van Der Straeten D (2014) 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: More than just the precursor of ethylene! Front. Plant Sci 5:640

    Google Scholar 

  • Vanderstraeten L, Depaepe T, Bertrand S et al (2019) The ethylene precursor ACC affects vegetative development independently of ethylene signaling. Front. Plant Sci 10:1591

    Google Scholar 

  • Vanderstraeten L, Van Der Straeten D (2017) Accumulation and transport of 1-aminocyclopropane-1- carboxylic acid in plants: current status, considerations for future research and agronomic applications. Front Plant Sci 8:38

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang AQ, Yang LT, Wang ZZ et al (2005a) Cloning and sequence analysis of three members of ACC synthase gene family in sugarcane. J Trop Subtropical Bot 13(6):485–492 (in Chinese)

    CAS  Google Scholar 

  • Wang F, Cui X, Sun Y et al (2013) Ethylene signaling and regulation in plant growth and stress responses. Plant Cell Rep 32(7):1099–1109

    Article  CAS  PubMed  Google Scholar 

  • Wang NN, Shih MC, Li N (2005b) The GUS reporter-aided analysis of the promoter activities of Arabidopsis ACC synthase genes AtACS4, AtACS5, and AtACS7 induced by hormones and stresses. J Exp Bot 56(413):909–920

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Wu H, Liu JH (2017) Genome-wide identification and expression profiling of copper-containing amine oxidase genes in sweet orange (Citrus sinensis). Tree Genet Genomes 13(2):31

    Article  Google Scholar 

  • Wang Y, Hua X, Xu J et al (2019) Comparative genomics revealed the gene evolution and functional divergence of magnesium transporter families in Saccharum. BMC Genomics 20(1):1–18

    Google Scholar 

  • Wang Y, Tang H, Debarry JD et al (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity.Nucleic Acids. Res.40(7), e49

  • Wang G, Kong H, Sun Y et al (2004) Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol 135(2):1084–1099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei LD, Chen W, Zhou Y et al (2015) Analysis on NPK-nutrient characteristics in shoot of different sugarcane genotypes. Sugarcane Canesugar 4:10–15 (in Chinese)

    Google Scholar 

  • Xing YZ, Jiang Y, Tan Q et al (2013) Study on nitrogen, phosphorous and potassium accumulation and utilization for three sugarcane genotypes. Sugarcane Canesugar 1:10–13 (in Chinese)

    Google Scholar 

  • Xu C, Hao B, Sun G, Mei Y, Sun L, Sun Y et al (2021) Dual activities of ACC synthase: Novel clues regarding the molecular evolution of ACS genes. Sci Adv 7(46):g8752

    Article  Google Scholar 

  • Xu MH, Wang MH (2012) Genome-wide analysis of 1-amino-cyclopropane-1-carboxylate synthase gene family in Arabidopsis, rice, grapevine and poplar. Afr J Biotechnol 11(5):1106–1118

    CAS  Google Scholar 

  • Yamagami T, Tsuchisaka A, Yamada K et al (2003) Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J Biol Chem 278(49):49102–49112

    Article  CAS  PubMed  Google Scholar 

  • Ye L, Li L, Wang L et al (2015) MPK3/MPK6 are involved in iron deficiency-induced ethylene production in Arabidopsis. Front. Plant Sci 6:953

    Google Scholar 

  • Yin Y, Vafeados D, Tao Y et al (2005) A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120(2):249–259

    Article  CAS  PubMed  Google Scholar 

  • Zarembinski TI, Theologis A (1994) Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol 26(5):1579–1597

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Du W, Fan J, Yang X, Chen Q, Liu Y et al (2021) Genome-Wide Identification of the 1-Aminocyclopropane-1-carboxylic Acid Synthase (ACS) Genes and Their Possible Role in Sand Pear (Pyrus pyrifolia) Fruit Ripening. Horticulturae 7(10):401

    Article  Google Scholar 

  • Zhang J, Zhang X, Tang H et al (2018) Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat Genet 50(11):1565–1573

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Zhang Q, Li L et al (2019) Recent polyploidization events in three Saccharum founding species. Plant Biotechnol J 17(1):264–274

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Hu W, Zhu F et al (2016) Structure, phylogeny, allelic haplotypes and expression of sucrose transporter gene families in Saccharum. BMC Genomics 17(1):1–18

    CAS  Google Scholar 

  • Zhang T, Qiao Q, Zhong Y (2012) Detecting adaptive evolution and functional divergence in aminocyclopropane-1-carboxylate synthase (ACS) gene family. Comput Biol Chem 38:10–16

    Article  PubMed  Google Scholar 

  • Zhu JH, Xu J, Chang WJ et al (2015) Isolation and molecular characterization of 1-aminocyclopropane-1-carboxylic acid synthase genes in Hevea brasiliensis. Int J Mol Sci 16(2):4136–4149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors are grateful to the Center for Genomics and Biotechnology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University for providing access to Saccharum data.

Funding

This research was supported by the GDAS’ Project of Science and Technology Development (2019GDASYL-0103030), the National Key Research and Development Program of China (2018YFD1000503), the China Agricultural Research System (CARS201707), the Technical System Innovation Team for Sugarcane Sisal Industry of Guangdong Province (2022KJ104-05), and the National Natural Science Foundation of China (32072027).

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Authors and Affiliations

  1. Guangdong Sugarcane Genetic Improvement Engineering Centre, Institute of Nanfan & Seed Industry, Guangdong Academy of Sciences, Shiliugang Road No.10, Haizhu District, Guangzhou, Guangdong Province, 510316, China

    Zilin Wu, Xiangbo Zhang, Nannan Zhang, Xiaoning Gao, Xiaomin Feng, Qiaoying Zeng, Xinglong Chen, Jiayun Wu & Yongwen Qi

  2. Zhanjiang Research Center, Institute of Nanfan & Seed Industry, Guangdong Academy of Sciences, Zhanjiang, Guangdong Province, 524300, China

    Xiaoning Gao

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  1. Zilin Wu
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  2. Xiangbo Zhang
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  3. Nannan Zhang
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  4. Xiaoning Gao
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  5. Xiaomin Feng
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  6. Qiaoying Zeng
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  7. Xinglong Chen
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  8. Jiayun Wu
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  9. Yongwen Qi
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Contributions

ZW conceived and designed the study. ZW, XZ, and NZ performed the experiments. ZW, XG, XF, QZ, XC carried out the data analysis. ZW prepared the manuscript. JW and YQ performed a critical review of intellectual content. All authors have read, edited, and approved the current version of the manuscript.

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Correspondence to Yongwen Qi.

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Wu, Z., Zhang, X., Zhang, N. et al. Identification of ACC Synthetase Genes in Saccharum and their Expression Profiles During Plant Growth and in Response to Low-nitrogen Stress. Tropical Plant Biol. 15, 197–210 (2022). https://doi.org/10.1007/s12042-022-09316-8

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