Genome-wide identification of heavy-metal ATPases genes in Areca catechu: investigating their functionality under heavy metal exposure.
Areca catechu
HMA gene family
Abiotic stress
Gene expression profile
Heavy metal
Journal
BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807
Informations de publication
Date de publication:
31 May 2024
31 May 2024
Historique:
received:
16
04
2024
accepted:
26
05
2024
medline:
1
6
2024
pubmed:
1
6
2024
entrez:
31
5
2024
Statut:
epublish
Résumé
Heavy-metal ATPases (HMAs) play a vital role in plants, helping to transport heavy metal ions across cell membranes.However, insufficient data exists concerning HMAs genes within the Arecaceae family.In this study, 12 AcHMA genes were identified within the genome of Areca catechu, grouped into two main clusters based on their phylogenetic relationships.Genomic distribution analysis reveals that the AcHMA genes were unevenly distributed across six chromosomes. We further analyzed their physicochemical properties, collinearity, and gene structure.Furthermore, RNA-seq data analysis exhibited varied expressions in different tissues of A. catechu and found that AcHMA1, AcHMA2, and AcHMA7 were highly expressed in roots, leaves, pericarp, and male/female flowers. A total of six AcHMA candidate genes were selected based on gene expression patterns, and their expression in the roots and leaves was determined using RT-qPCR under heavy metal stress. Results showed that the expression levels of AcHMA1 and AcHMA3 genes were significantly up-regulated under Cd2 + and Zn2 + stress. Similarly, in response to Cu
Identifiants
pubmed: 38822228
doi: 10.1186/s12870-024-05201-6
pii: 10.1186/s12870-024-05201-6
doi:
Substances chimiques
Metals, Heavy
0
Adenosine Triphosphatases
EC 3.6.1.-
Plant Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
484Subventions
Organisme : Hainan Provincial Natural Science Foundation of China
ID : 2019RCI55
Informations de copyright
© 2024. The Author(s).
Références
Cao Y, Zhao X, Liu Y, Wang Y, Wu W, Jiang Y, et al. Genome-wide identification of ZmHMAs and association of natural variation in ZmHMA2 and ZmHMA3 with leaf cadmium accumulation in maize. PeerJ. 2019;7:e7877.
pubmed: 31660268
pmcid: 6815194
doi: 10.7717/peerj.7877
Razi K, Muneer S. Drought stress-induced physiological mechanisms, signaling pathways and molecular response of chloroplasts in common vegetable crops. Crit Rev Biotechnol. 2021;41:669–91.
pubmed: 33525946
doi: 10.1080/07388551.2021.1874280
Kumar S, Prasad S, Yadav KK, Shrivastava M, Gupta N, Nagar S, et al. Hazardous heavy metals contamination of vegetables and food chain: role of sustainable remediation approaches - a review. Environ Res. 2019;179:108792.
pubmed: 31610391
doi: 10.1016/j.envres.2019.108792
Kosakivska IV, Babenko LM, Romanenko KO, Korotka IY, Potters G. Molecular mechanisms of plant adaptive responses to heavy metals stress. Cell Biol Int. 2021;45:258–72.
pubmed: 33200493
doi: 10.1002/cbin.11503
Jamla M, Khare T, Joshi S, Patil S, Penna S, Kumar V. Omics approaches for understanding heavy metal responses and tolerance in plants. Curr Plant Biol. 2021;27:100213.
doi: 10.1016/j.cpb.2021.100213
Htwe T, Onthong J, Duangpan S, Techato K, Chotikarn P, Sinutok S. Effect of copper contamination on plant growth and metal contents in Rice Plant (Oryza Sativa L). Commun Soil Sci Plant Anal. 2020;51:2349–60.
doi: 10.1080/00103624.2020.1836200
Chmur M, Bajguz A. Melatonin involved in Protective effects against Cadmium stress in Wolffia arrhiza. Int J Mol Sci. 2023;24.
Vatansever R, Ozyigit II, Filiz E. Essential and Beneficial Trace Elements in Plants, and their transport in roots: a review. Appl Biochem Biotechnol. 2017;181:464–82.
pubmed: 27687587
doi: 10.1007/s12010-016-2224-3
Li G, Li C, Rengel Z, Liu H, Zhao P. Title: excess Zn-induced changes in physiological parameters and expression levels of TaZips in two wheat genotypes. Environ Exp Bot. 2020;177:104133.
doi: 10.1016/j.envexpbot.2020.104133
Nedjimi B. Phytoremediation: a sustainable environmental technology for heavy metals decontamination. SN Appl Sci. 2021;3:286.
doi: 10.1007/s42452-021-04301-4
Hall JL. Transition metal transporters in plants. J Exp Bot. 2003;54:2601–13.
pubmed: 14585824
doi: 10.1093/jxb/erg303
Ray S, Gaudet R. Structures and coordination chemistry of transporters involved in manganese and iron homeostasis. Biochem Soc Trans. 2023;51:897–923.
pubmed: 37283482
doi: 10.1042/BST20210699
Wu D, Saleem M, He T, He G. The mechanism of metal homeostasis in plants: a New View on the synergistic regulation pathway of membrane proteins, lipids and metal ions. Membr (Basel). 2021;11:984.
Williams LE, Mills RF. P1B-ATPases - an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci. 2005;10:491–502.
pubmed: 16154798
doi: 10.1016/j.tplants.2005.08.008
Huang Q, Qiu W, Yu M, Li S, Lu Z, Zhu Y, et al. Genome-wide characterization of Sedum Plumbizincicola HMA Gene Family provides functional implications in Cadmium Response. Plants. 2022;11:215.
pubmed: 35050103
pmcid: 8779779
doi: 10.3390/plants11020215
Wu Y, Li X, Chen D, Han X, Li B, Yang Y, et al. Comparative expression analysis of heavy metal ATPase subfamily genes between Cd-tolerant and Cd-sensitive turnip landraces. Plant Divers. 2019;41:275–83.
pubmed: 31528787
pmcid: 6742492
doi: 10.1016/j.pld.2019.02.001
Smith AT, Smith KP, Rosenzweig AC. Diversity of the metal-transporting P1B-type ATPases. JBIC J Biol Inorg Chem. 2014;19:947–60.
pubmed: 24729073
doi: 10.1007/s00775-014-1129-2
Fang X, Wang L, Deng X, Wang P, Ma Q, Nian H, et al. Genome-wide characterization of soybean P 1B -ATPases gene family provides functional implications in cadmium responses. BMC Genomics. 2016;17:1–15.
doi: 10.1186/s12864-016-2730-2
Batool TS, Aslam R, Gul A, Paracha RZ, Ilyas M, De Abreu K, et al. Genome-wide analysis of heavy metal ATPases (HMAs) in Poaceae species and their potential role against copper stress in Triticum aestivum. Sci Rep. 2023;13:1–13.
doi: 10.1038/s41598-023-32023-7
Takahashi R, Bashir K, Ishimaru Y, Nishizawa NK, Nakanishi H. Takahashi (‘12) - The role of heavy-metal ATPases, HMAs, in zinc. 2012; December:1605–7.
Zhiguo E, Tingting L, Chen C, Lei W. Genome-wide survey and expression analysis of P 1B -ATPases in Rice, Maize and Sorghum. Rice Sci. 2018;25:208–17.
doi: 10.1016/j.rsci.2018.06.004
Zahra S, Shaheen T, Qasim M, Mahmood-Ur-Rahman, Hussain M, Zulfiqar S, et al. Genome-wide survey of HMA gene family and its characterization in wheat (Triticum aestivum). PeerJ. 2023;11:1–20.
doi: 10.7717/peerj.14920
Kim Y, Choi H, Segami S, Cho H, Martinoia E, Maeshima M, et al. AtHMA1 contributes to the detoxification of excess zn(II) in Arabidopsis. Plant J. 2009;58:737–53.
pubmed: 19207208
doi: 10.1111/j.1365-313X.2009.03818.x
Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, Sakurai K, et al. Mutations in rice (oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 2012;53:213–24.
pubmed: 22123790
doi: 10.1093/pcp/pcr166
Fan W, Liu C, Cao B, Qin M, Long D, Xiang Z, et al. Genome-wide identification and characterization of four gene families putatively involved in cadmium uptake, translocation and sequestration in mulberry. Front Plant Sci. 2018;9:1–16.
doi: 10.3389/fpls.2018.00879
Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, et al. AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb Vacuolar Storage in Arabidopsis. Plant Physiol. 2009;149:894–904.
pubmed: 19036834
pmcid: 2633814
doi: 10.1104/pp.108.130294
Suzuki M, Bashir K, Inoue H, Takahashi M, Nakanishi H, Nishizawa NK. Accumulation of starch in Zn-deficient rice. Rice. 2012;5:9.
pubmed: 27234235
pmcid: 5520845
doi: 10.1186/1939-8433-5-9
Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, et al. Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci. 2010;107:16500–5.
pubmed: 20823253
pmcid: 2944702
doi: 10.1073/pnas.1005396107
Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, et al. OsHMA3, a P 1B -type of ATPase affects root‐to‐shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol. 2011;189:190–9.
pubmed: 20840506
doi: 10.1111/j.1469-8137.2010.03459.x
Yan J, Wang P, Wang P, Yang M, Lian X, Tang Z, et al. A loss-of‐function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars. Plant Cell Environ. 2016;39:1941–54.
pubmed: 27038090
doi: 10.1111/pce.12747
Salehi B, Konovalov DA, Fru P, Kapewangolo P, Peron G, Ksenija MS, et al. Areca catechu —from farm to food and biomedical applications. Phyther Res. 2020;34:2140–58.
doi: 10.1002/ptr.6665
Zhou G, Yin H, Chen F, Wang Y, Gao Q, Yang F, et al. The genome of Areca catechu provides insights into sex determination of monoecious plants. New Phytol. 2022;236:2327–43.
pubmed: 36089819
doi: 10.1111/nph.18471
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, et al. TBtools: an integrative Toolkit developed for interactive analyses of big Biological Data. Mol Plant. 2020;13:1194–202.
pubmed: 32585190
doi: 10.1016/j.molp.2020.06.009
Nazmul Hasan M, Islam S, Bhuiyan FH, Arefin S, Hoque H, Azad Jewel N et al. Genome wide analysis of the heavy-metal-associated (HMA) gene family in tomato and expression profiles under different stresses. Gene. 2022;835 November 2021:146664.
Hall JL. Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot. 2002;53:1–11.
pubmed: 11741035
doi: 10.1093/jexbot/53.366.1
Palmgren MG, Nissen P. P-Type ATPases. Annu Rev Biophys. 2011;40:243–66.
pubmed: 21351879
doi: 10.1146/annurev.biophys.093008.131331
Williams LE, Mills RF. P1B-ATPases – an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci. 2005;10:491–502.
Takahashi R, Bashir K, Ishimaru Y, Nishizawa NK, Nakanishi H. The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signal Behav. 2012;7:1605–7.
pubmed: 23072989
pmcid: 3578901
doi: 10.4161/psb.22454
Li D, Xu X, Hu X, Liu Q, Wang Z, Zhang H, et al. Genome-wide analysis and heavy metal-induced expression profiling of the HMA gene family in populus trichocarpa. Front Plant Sci. 2015;6 DEC:1–15.
Fang X, Wang L, Deng X, Wang P, Ma Q, Nian H, et al. Genome-wide characterization of soybean P 1B -ATPases gene family provides functional implications in cadmium responses. BMC Genomics. 2016;17:376.
pubmed: 27207280
pmcid: 4874001
doi: 10.1186/s12864-016-2730-2
Li N, Xiao H, Sun J, Wang S, Wang J, Chang P, et al. Genome-wide analysis and expression profiling of the HMA gene family in Brassica napus under cd stress. Plant Soil. 2018;426:365–81.
doi: 10.1007/s11104-018-3637-2
Zhang C, Yang Q, Zhang X, Zhang X, Yu T, Wu Y et al. Genome-wide identification of the HMA gene family and expression analysis under cd stress in barley. Plants. 2021;10.
43. Wu Y, Li X, Chen D, Han X, Li B, Yang Y, et al. Comparative expression analysis of heavy metal ATPase subfamily genes between Cd-tolerant and Cd-sensitive turnip landraces. Plant Divers. 2019;41:275–83.
Li J, Zhang M, Sun J, Mao X, Wang J, Liu H, et al. Heavy Metal Stress-Associated Proteins in Rice and Arabidopsis: genome-wide identification, Phylogenetics, Duplication, and expression profiles analysis. Front Genet. 2020;11:1–21.
Khan N, You FM, Datla R, Ravichandran S, Jia B, Cloutier S. Genome-wide identification of ATP binding cassette (ABC) transporter and heavy metal associated (HMA) gene families in flax (Linum usitatissimum L). BMC Genomics. 2020;21:1–22.
doi: 10.1186/s12864-020-07121-9
Wang Q, Lu X, Chen X, Zhao L, Han M, Wang S, et al. Genome-wide identification and function analysis of HMAD gene family in cotton (Gossypium spp). BMC Plant Biol. 2021;21:386.
pubmed: 34416873
pmcid: 8377987
doi: 10.1186/s12870-021-03170-8
Zaman QU, Hussain MA, Khan LU, Hui L, Khan D, Khokhar AA, et al. Genome-wide identification and expression profiling of APX gene family under multifactorial stress combinations and melatonin-mediated tolerance in pitaya. Sci Hortic (Amsterdam). 2023;321:112312.
doi: 10.1016/j.scienta.2023.112312
Gao C, Gao K, Yang H, Ju T, Zhu J, Tang Z, et al. Genome-wide analysis of metallothionein gene family in maize to reveal its role in development and stress resistance to heavy metal. Biol Res. 2022;55:1.
pubmed: 35012672
pmcid: 8751047
doi: 10.1186/s40659-021-00368-w
Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, et al. HMA1, a New Cu-ATPase of the Chloro plast envelope, is essential for growth under adverse light conditions. J Biol Chem. 2006;281:2882–92.
pubmed: 16282320
doi: 10.1074/jbc.M508333200
Lee S, Kim Y-Y, Lee Y, An G. Rice P1B-Type Heavy-Metal ATPase, OsHMA9, is a metal efflux protein. Plant Physiol. 2007;145:831–42.
pubmed: 17827266
pmcid: 2048805
doi: 10.1104/pp.107.102236
Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK. The OsHMA2 transporter is involved in root-to‐shoot translocation of Zn and Cd in rice. Plant Cell Environ. 2012;35:1948–57.
pubmed: 22548273
doi: 10.1111/j.1365-3040.2012.02527.x
Deng F, Yamaji N, Xia J, Ma JF. A Member of the heavy metal P-Type ATPase OsHMA5 is involved in Xylem Loading of copper in Rice. Plant Physiol. 2013;163:1353–62.
pubmed: 24064929
pmcid: 3813655
doi: 10.1104/pp.113.226225
Huang X-Y, Deng F, Yamaji N, Pinson SRM, Fujii-Kashino M, Danku J, et al. A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. Nat Commun. 2016;7:12138.
pubmed: 27387148
pmcid: 4941113
doi: 10.1038/ncomms12138
Smith AT, Barupala D, Stemmler TL, Rosenzweig AC. A new metal binding domain involved in cadmium, cobalt and zinc transport. Nat Chem Biol. 2015;11:678–84.
pubmed: 26192600
pmcid: 4543396
doi: 10.1038/nchembio.1863
Arnesano F, Banci L, Bertini I, Ciofi-Baffoni S, Molteni E, Huffman DL, et al. Metallochaperones and metal-transporting ATPases: a comparative analysis of sequences and structures. Genome Res. 2002;12:255–71.
pubmed: 11827945
doi: 10.1101/gr.196802
Furukawa Y, Lim C, Tosha T, Yoshida K, Hagai T, Akiyama S, et al. Identification of a novel zinc-binding protein, C1orf123, as an interactor with a heavy metal-associated domain. PLoS ONE. 2018;13:e0204355.
pubmed: 30260988
pmcid: 6160046
doi: 10.1371/journal.pone.0204355
Liu H, Zhao H, Wu L, Liu A, Zhao F, Xu W. Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol. 2017;215Heavy m:687–98.
Xu G, Guo C, Shan H, Kong H. Divergence of duplicate genes in exon–intron structure. Proc Natl Acad Sci. 2012;109:1187–92.
pubmed: 22232673
pmcid: 3268293
doi: 10.1073/pnas.1109047109
Zhu L, Zhang Y, Zhang W, Yang S, Chen J-Q, Tian D. Patterns of exon-intron architecture variation of genes in eukaryotic genomes. BMC Genomics. 2009;10:47.
pubmed: 19166620
pmcid: 2636830
doi: 10.1186/1471-2164-10-47
Marand AP, Eveland AL, Kaufmann K, Springer NM. cis -Regulatory Elements in Plant Development, Adaptation, and evolution. Annu Rev Plant Biol. 2023;74:111–37.
pubmed: 36608347
pmcid: 9881396
doi: 10.1146/annurev-arplant-070122-030236
Sabagh EL, Islam A, Hossain MS, Iqbal A, Mubeen MA, Waleed M. M, Phytohormones as growth regulators during abiotic stress tolerance in plants. Front Agron. 2022;4.
Singh S, Parihar P, Singh R, Singh VP, Prasad SM. Heavy metal tolerance in plants: role of Transcriptomics, Proteomics, Metabolomics, and Ionomics. Front Plant Sci. 2016;6.
Melo BP de, de Moura SM, Morgante CV, Pinheiro DH, Alves NSF, Rodrigues-Silva PL, et al. Regulated promoters applied to plant engineering: an insight over promising soybean promoters under biotic stress and their cis-elements. Biotechnol Res Innov. 2021;5:e2021005.
doi: 10.4322/biori.202105