Identification and characterization of PAL genes involved in the regulation of stem development in Saccharum spontaneum L.


Journal

BMC genomic data
ISSN: 2730-6844
Titre abrégé: BMC Genom Data
Pays: England
ID NLM: 101775394

Informations de publication

Date de publication:
30 Apr 2024
Historique:
received: 11 01 2024
accepted: 12 03 2024
medline: 1 5 2024
pubmed: 1 5 2024
entrez: 30 4 2024
Statut: epublish

Résumé

Saccharum spontaneum L. is a closely related species of sugarcane and has become an important genetic component of modern sugarcane cultivars. Stem development is one of the important factors for affecting the yield, while the molecular mechanism of stem development remains poorly understanding in S. spontaneum. Phenylalanine ammonia-lyase (PAL) is a vital component of both primary and secondary metabolism, contributing significantly to plant growth, development and stress defense. However, the current knowledge about PAL genes in S. spontaneum is still limited. Thus, identification and characterization of the PAL genes by transcriptome analysis will provide a theoretical basis for further investigation of the function of PAL gene in sugarcane. In this study, 42 of PAL genes were identified, including 26 SsPAL genes from S. spontaneum, 8 ShPAL genes from sugarcane cultivar R570, and 8 SbPAL genes from sorghum. Phylogenetic analysis showed that SsPAL genes were divided into three groups, potentially influenced by long-term natural selection. Notably, 20 SsPAL genes were existed on chromosomes 4 and 5, indicating that they are highly conserved in S. spontaneum. This conservation is likely a result of the prevalence of whole-genome replications within this gene family. The upstream sequence of PAL genes were found to contain conserved cis-acting elements such as G-box and SP1, GT1-motif and CAT-box, which collectively regulate the growth and development of S. spontaneum. Furthermore, quantitative reverse transcription polymerase chain reaction (qRT-PCR) analysis showed that SsPAL genes of stem had a significantly upregulated than that of leaves, suggesting that they may promote the stem growth and development, particularly in the + 6 stem (The sixth cane stalk from the top to down) during the growth stage. The results of this study revealed the molecular characteristics of SsPAL genes and indicated that they may play a vital role in stem growth and development of S. spontaneum. Altogether, our findings will promote the understanding of the molecular mechanism of S. spontaneum stem development, and also contribute to the sugarcane genetic improving.

Sections du résumé

BACKGROUND BACKGROUND
Saccharum spontaneum L. is a closely related species of sugarcane and has become an important genetic component of modern sugarcane cultivars. Stem development is one of the important factors for affecting the yield, while the molecular mechanism of stem development remains poorly understanding in S. spontaneum. Phenylalanine ammonia-lyase (PAL) is a vital component of both primary and secondary metabolism, contributing significantly to plant growth, development and stress defense. However, the current knowledge about PAL genes in S. spontaneum is still limited. Thus, identification and characterization of the PAL genes by transcriptome analysis will provide a theoretical basis for further investigation of the function of PAL gene in sugarcane.
RESULTS RESULTS
In this study, 42 of PAL genes were identified, including 26 SsPAL genes from S. spontaneum, 8 ShPAL genes from sugarcane cultivar R570, and 8 SbPAL genes from sorghum. Phylogenetic analysis showed that SsPAL genes were divided into three groups, potentially influenced by long-term natural selection. Notably, 20 SsPAL genes were existed on chromosomes 4 and 5, indicating that they are highly conserved in S. spontaneum. This conservation is likely a result of the prevalence of whole-genome replications within this gene family. The upstream sequence of PAL genes were found to contain conserved cis-acting elements such as G-box and SP1, GT1-motif and CAT-box, which collectively regulate the growth and development of S. spontaneum. Furthermore, quantitative reverse transcription polymerase chain reaction (qRT-PCR) analysis showed that SsPAL genes of stem had a significantly upregulated than that of leaves, suggesting that they may promote the stem growth and development, particularly in the + 6 stem (The sixth cane stalk from the top to down) during the growth stage.
CONCLUSIONS CONCLUSIONS
The results of this study revealed the molecular characteristics of SsPAL genes and indicated that they may play a vital role in stem growth and development of S. spontaneum. Altogether, our findings will promote the understanding of the molecular mechanism of S. spontaneum stem development, and also contribute to the sugarcane genetic improving.

Identifiants

pubmed: 38689211
doi: 10.1186/s12863-024-01219-9
pii: 10.1186/s12863-024-01219-9
doi:

Substances chimiques

Phenylalanine Ammonia-Lyase EC 4.3.1.24
Plant Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

38

Informations de copyright

© 2024. The Author(s).

Références

Parameswari B, Nithya K, Kumar S et al. Genome wide association studies in sugarcane host pathogen system for disease resistance: an update on the current status of research[J]. Indian Phytopathol, 2021(5).
Dal-Bianco M, Carneiro MS, Hotta CT, Chapola RG, Hoffmann HP. Sugarcane improvement: how far can we go? Curr Opin Biotechnol. 2012;23(2):265–70.
pubmed: 21983270 doi: 10.1016/j.copbio.2011.09.002
Moore PH. Temporal and spatial regulation of sucrose accumulation in the sugarcane stem. Funct Plant Biol. 1995;22(4):661–79.
doi: 10.1071/PP9950661
Zhang Q, Qi Y, Pan H, Tang H, Wang G, Hua X. Genomic insights into the recent chromosome reduction of autopolyploid sugarcane Saccharum spontaneum. Nat Genet. 2022;54(6):885–96.
pubmed: 35654976 doi: 10.1038/s41588-022-01084-1
da Silva JA. The importance of the Wild Cane Saccharum spontaneum for Bioenergy genetic breeding. Sugar Tech. 2017;19(3):229–40.
doi: 10.1007/s12355-017-0510-1
Yu F, Wang P, Li X, Huang Y, Wang Q. Characterization of chromosome composition of sugarcane in nobilization by using genomic in situ hybridization. Mol Cytogenet. 2018;11(1):35.
pubmed: 29977338 pmcid: 5992832 doi: 10.1186/s13039-018-0387-z
D’Hont A, Grivet L, Feldmann P, Glaszmann JC, Rao S, Berding N. Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp) by molecular cytogenetics. Mol Gen Genet MGG. 1996;250(4):405–13.
pubmed: 8602157 doi: 10.1007/s004380050092
Piperidis G, Piperidis N, D’Hont A. Molecular cytogenetic investigation of chromosome composition and transmission in sugarcane. Mol Genet Genomics. 2010;284(1):65–73.
pubmed: 20532565 doi: 10.1007/s00438-010-0546-3
Feng YT, Huang QL, Zhang R. Molecular characterisation of PAL gene family reveals their role in abiotic stress response in lucerne (Medicago sativa). Crop Pasture Sci. 2022;73(3):300–11.
doi: 10.1071/CP21558
Vogt T. Phenylpropanoid Biosynthesis. Mol Plant. 2010;3(1):2–20.
pubmed: 20035037 doi: 10.1093/mp/ssp106
Tonnessen, Bradley W, et al. Rice phenylalanine ammonia-lyase gene OsPAL4 is associated with broad spectrum disease resistance. Plant Mol Biol. 2015;87(3):273–86.
pubmed: 25515696 doi: 10.1007/s11103-014-0275-9
Xiao-Zhang Y, Wei-Jia F,,Yu-Juan L et al. Differential expression of the PAL gene family in rice seedlings exposed to chromium by microarray analysis.[J].Ecotoxicology (London, England),2018,27(3):325–335.
Dehghan S, Sadeghi M, Pöppel A. Differential inductions of phenylalanine ammonia-lyase and chalcone synthase during wounding, salicylic acid treatment, and salinity stress in safflower, Carthamus tinctorius. Biosci Rep 2014, 34(3).
Raes J, Rohde A, Christensen JH. Genome-wide characterization of the Lignification Toolbox in Arabidopsis. Plant Physiol. 2003;133(3):1051–71.
pubmed: 14612585 pmcid: 523881 doi: 10.1104/pp.103.026484
Reichert Angelika I, He X-Z, Dixon Richard A. Phenylalanine ammonia-lyase (PAL) from tobacco (Nicotiana tabacum): characterization of the four tobacco PAL genes and active heterotetrameric enzymes1. Biochem J. 2009;424(2):233–42.
pubmed: 19725811 doi: 10.1042/BJ20090620
Tonnessen BW, Manosalva P, Lang JM. Rice phenylalanine ammonia-lyase gene OsPAL4 is associated with broad spectrum disease resistance. Plant Mol Biol. 2015;87(3):273–86.
pubmed: 25515696 doi: 10.1007/s11103-014-0275-9
Yan F, Li H, Zhao P. Genome-wide identification and transcriptional expression of the PAL Gene Family in Common Walnut (Juglans Regia L). Genes. 2019;10(1):46.
pubmed: 30650597 pmcid: 6357058 doi: 10.3390/genes10010046
Mo F, Li L, Zhang C. Genome-wide analysis and expression profiling of the phenylalanine Ammonia-lyase Gene Family in Solanum tuberosum. Int J Mol Sci. 2022;23(12):6833.
pubmed: 35743276 pmcid: 9224352 doi: 10.3390/ijms23126833
Li G, Wang H, Cheng X. Comparative genomic analysis of the PAL genes in five Rosaceae species and functional identification of Chinese white pear. PeerJ. 2019;7:e8064.
pubmed: 31824757 pmcid: 6894436 doi: 10.7717/peerj.8064
Chen YP, Li FJ, Tian L. The phenylalanine Ammonia Lyase Gene LjPAL1 is involved in plant defense responses to Pathogens and Plays Diverse roles in Lotus japonicus-Rhizobium Symbioses. Mol Plant Microbe Interact. 2017;30(9):739–53.
pubmed: 28598263 doi: 10.1094/MPMI-04-17-0080-R
Bagal UR, Leebens-Mack JH, Lorenz WW. The phenylalanine ammonia lyase (PAL) gene family shows a gymnosperm-specific lineage. BMC Genomics 2012, 13.
He J, Liu YQ, Yuan DY. An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice. Proc Natl Acad Sci USA. 2020;117(1):271–7.
pubmed: 31848246 doi: 10.1073/pnas.1902771116
Yuan Y, Yang X, Feng M. Genome-wide analysis of R2R3-MYB transcription factors family in the autopolyploid Saccharum spontaneum: an exploration of dominance expression and stress response. BMC Genomics. 2021;22:1–18.
doi: 10.1186/s12864-021-07689-w
Qin Y, Li QE, An QJ. A phenylalanine ammonia lyase from Fritillaria unibracteata promotes drought tolerance by regulating lignin biosynthesis and SA signaling pathway. Int J Biol Macromol. 2022;213:574–88.
pubmed: 35643154 doi: 10.1016/j.ijbiomac.2022.05.161
Gho YS, Kim SJ, Jung KH. Phenylalanine ammonia-lyase family is closely associated with response to phosphate deficiency in rice. Genes Genomics. 2020;42(1):67–76.
pubmed: 31736007 doi: 10.1007/s13258-019-00879-7
Zhao SS, Zhao L, Liu FX. NARROW AND ROLLED LEAF 2 regulates leaf shape, male fertility, and seed size in rice. J Integr Plant Biol. 2016;58(12):983–96.
pubmed: 27762074 doi: 10.1111/jipb.12503
Huang J, Gu M, Lai Z. Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol. 2010;153(4):1526–38.
pubmed: 20566705 pmcid: 2923909 doi: 10.1104/pp.110.157370
Pourcel L, Routaboul JM, Cheynier V. Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci. 2007;12(1):29–36.
pubmed: 17161643 doi: 10.1016/j.tplants.2006.11.006
Panche AN, Diwan AD, Chandra SR. Flavonoids: an overview. J Nutritional Sci. 2016;5:e47.
doi: 10.1017/jns.2016.41
Santos-Buelga C, Mateus N, Freitas D. Anthocyanins. Plant pigments and beyond. In., vol. 62. Journal of agricultural food chemistry: ACS Publications; 2014: 6879–6884.
Zhang ZC, Sun CQ, Yao YM. Red anthocyanins contents and the relationships with phenylalanine ammonia lyase (PAL) activity, soluble sugar and chlorophyll contents in carmine radish (Raphanus sativus L). Hortic Sci. 2019;46(1):17–25.
doi: 10.17221/202/2017-HORTSCI
Ritter H, Schulz GE. Structural basis for the entrance into the phenylpropanoid metabolism catalyzed by phenylalanine ammonia-lyase. Plant Cell. 2004;16(12):3426–36.
pubmed: 15548745 pmcid: 535883 doi: 10.1105/tpc.104.025288
Zhang J, Zhang X, Tang H. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L[J]. Nat Genet. 2018;50(11):1565–73.
pubmed: 30297971 doi: 10.1038/s41588-018-0237-2
Garsmeur O, Droc G, Antonise R. A mosaic monoploid reference sequence for the highly complex genome of sugarcane. Nat Commun. 2018;9(1):2638.
pubmed: 29980662 pmcid: 6035169 doi: 10.1038/s41467-018-05051-5
Wheeler TJ, Eddy SR. Nhmmer: DNA homology search with profile HMMs. Bioinformatics. 2013;29(19):2487–9.
pubmed: 23842809 pmcid: 3777106 doi: 10.1093/bioinformatics/btt403
Finn RD, Coggill P, Eberhardt RY. The pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 2016;44(D1):D279–85.
pubmed: 26673716 doi: 10.1093/nar/gkv1344
Bailey TL, Johnson J, Grant CE. The MEME suite. Nucleic Acids Res. 2015;43(W1):W39–49.
pubmed: 25953851 pmcid: 4489269 doi: 10.1093/nar/gkv416
Lescot M, Déhais P, Thijs G. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30(1):325–7.
pubmed: 11752327 pmcid: 99092 doi: 10.1093/nar/30.1.325
Wang Y, Tang H, Debarry JD. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012;40(7):e49–49.
pubmed: 22217600 pmcid: 3326336 doi: 10.1093/nar/gkr1293
Chen C, Chen H, Zhang Y. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13(8):1194–202.
pubmed: 32585190 doi: 10.1016/j.molp.2020.06.009
Li Z, Hua X, Zhong W. Genome-wide identification and expression profile analysis of WRKY family genes in the autopolyploid Saccharum spontaneum. Plant Cell Physiol. 2020;61(3):616–30.
pubmed: 31830269 doi: 10.1093/pcp/pcz227
Ling H, Wu Q, Guo J, Xu L, Que Y. Comprehensive Selection of reference genes for gene expression normalization in sugarcane by Real Time quantitative RT-PCR. PLoS ONE. 2014;9(5):e97469.
pubmed: 24823940 pmcid: 4019594 doi: 10.1371/journal.pone.0097469
SONG X P, HUANG X, MO F L et al. Cloning and expression analysis of sugarcane phenylalanin ammonia-lyase(PAL) gene [J]. Scientia Agricultura Sinica, 2013, 46(14): 2856–2868.
Li Y, Xihe Z, Kai Y, et al. Physiological mechanism of different varieties and potassium application amount on cotton resistance to Verticillium wilt[J]. Cotton Sci. 2019;31(1):40–53.
Valcarcel J, et al. Levels of potential bioactive compounds including carotenoids, vitamin C and phenolic compounds, and expression of their cognate biosynthetic genes vary significantly in different varieties of potato (Solanum tuberosum L.) grown under uniform cultural conditions. J Sci food Agric vol. 2016;96(3):1018–26.
doi: 10.1002/jsfa.7189
Xuejin Chen B. A, Identification of PAL genes related to anthocyanin synthesis in tea plants and its correlation with anthocyanin content. Hortic Plant J 8. 3(2022):381–94.
Huang J et al. Functional analysis of the ArabidopsisPALGene Family in Plant Growth, Development, and response to environmental stress. Plant Physiol 153.4(2010):1526–38.
Reichert A, He XZ, Dixon R. Phenylalanine ammonia-lyase (pal) from tobacco (nicotiana tabacum): characterization of the four tobacco pal genes and active heterotetrameric enzymes. Biochem J, 424(2), 233–42.
Pant S, Huang Y. genes in sorghum and their responses to aphid infestation[J].Scientific Reports.
Hamberger B, et al. Genome-wide analyses of phenylpropanoid-related genes in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families. Can J Bot. 2007;85:1182–201.
doi: 10.1139/B07-098
Shang QM, Li L, Dong CJ. Multiple tandem duplication of the phenylalanine ammonia-lyase genes in Cucumis sativus L. Planta. 2012;236(4):1093–105.
pubmed: 22572777 doi: 10.1007/s00425-012-1659-1
Wu D-G, Yu ZHANQ. Genome-wide identification and analysis of maize pal gene family and its expression profile in response to high-temperature stress. Pak J Bot. 2020;52(5):1577–87.
doi: 10.30848/PJB2020-5(28)
Rasool F, Uzair M, Naeem MK. Phenylalanine Ammonia-lyase (PAL) genes family in wheat (Triticum aestivum L). Genome-Wide Charact Expression Profiling. 2021;11(12):2511.
Clark JW, Donoghue PCJ. Whole-genome duplication and plant macroevolution. Trends Plant Sci. 2018;23(10):933–45.
pubmed: 30122372 doi: 10.1016/j.tplants.2018.07.006
Fukasawa-Akada T, Kung SD, Watson JC. Phenylalanine ammonia-lyase gene structure, expression, and evolution in Nicotiana. Plant Mol Biol. 1996;30(4):711–22.
pubmed: 8624404 doi: 10.1007/BF00019006
LI Q E, QIN Y, ZHENG Q M, et al. Codon bias and evolution analysis of phenylalanine ammonia-lyase gene [J]. J Biol. 2022;39(3):36–40.
Rongrong L, Shaohua X,,Jialin L et al. Expression profile of a PAL gene from Astragalus membranaceus var. Mongholicus and its crucial role in flux into flavonoid biosynthesis.[J].Plant cell reports,2006,25(7):705–10.
Pellegrini L, Rohfritsch O, Fritig B, et al. Phenylalanine ammonia-lyase in tobacco: molecular cloning and gene expression during the hypersensitive reaction to tobacco mosaic virus and the response to a fungal elicitor [. J] Plant Physiol. 1994;106(3):877–86.
pmcid: 159610 doi: 10.1104/pp.106.3.877
Cochrane FC, Davin LB, Lewis NG. The Arabidopsis phenylalanine ammonia lyase gene family: kinetic characterization of the four PAL isoforms. Phytochemistry. 2004;65(11):1557–64.
pubmed: 15276452 doi: 10.1016/j.phytochem.2004.05.006

Auteurs

Xiaoqing Wu (X)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China.

Zetian Cui (Z)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China.

Xinyi Li (X)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China.

Zehuai Yu (Z)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China.

Pingping Lin (P)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China.

Li Xue (L)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China.

Abdullah Khan (A)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China.

Cailan Ou (C)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China.

Zuhu Deng (Z)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China.
National Engineering Research Center for Sugarcane, Fujian Agriculture and Forestry University, Fuzhou, Fujian, 350002, China.
Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University, Fuzhou, 350002, China.

Muqing Zhang (M)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China.

Wei Yao (W)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China. yaoweimail@163.com.

Fan Yu (F)

State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi Key Laboratory for Sugarcane Biology, Academy of Sugarcane and Sugar Industry, Guangxi University, Nanning, 530004, China. yufanky@163.com.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family

Classifications MeSH