Abstract
Hsp70 proteins function as molecular chaperones, regulating various cellular processes in plants. In this study, a genome-wide analysis led to the identification of 22 Hsp70 (MeHsp70) genes in cassava. Phylogenetic relationship studies with other Malpighiales genomes (Populus trichocarpa, Ricinus communis and Salix purpurea) classified MeHsp70 proteins into eight groups (Ia, Ib, Ic, Id, Ie, If, IIa and IIb). Promoter analysis of MeHsp70 genes revealed the presence of tissue-specific, light, biotic and abiotic stress-responsive cis-regulatory elements showing their functional importance in cassava. Meta-analysis of publically available RNA-seq transcriptome datasets showed constitutive, tissue-specific, biotic and abiotic stress-specific expression patterns among MeHsp70s in cassava. Among 22 Hsp70, six MeHsp70s viz., MecHsp70-3, MecHsp70-6, MeBiP-1, MeBiP-2, MeBiP-3 and MecpHsp70-2 displayed constitutive expression, while three MecHsp70s were induced under both drought and cold stress conditions. Five MeHsp70s, MecHsp70-7, MecHsp70-11, MecHsp70-12, MecHsp70-13, and MecHsp70-14 were induced under drought stress conditions. We predicted that 19 MeHsp70 genes are under the regulation of 24 miRNAs. This comprehensive genome-wide analysis of the Hsp70 gene family in cassava provided valuable insights into their functional roles and identified various potential Hsp70 genes associated with stress tolerance and adaptation to environmental stimuli.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbas M, Li Y, Elbaiomy RG et al (2022) Genome-wide analysis and expression profiling of SlHsp70 gene family in Solanum lycopersicum revealed higher expression of SlHsp70–11 in roots under Cd2+ Stress. Front Biosci Landmark 27:186. https://doi.org/10.31083/j.fbl2706186
Arhar T, Shkedi A, Nadel CM, Gestwicki JE (2021) The interactions of molecular chaperones with client proteins: why are they so weak? J Biol Chem 297:101282. https://doi.org/10.1016/j.jbc.2021.101282
Artimo P, Jonnalagedda M, Arnold K et al (2012) ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res 40:W597-603. https://doi.org/10.1093/nar/gks400
Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME Suite. Nucleic Acids Res 43:W39-49. https://doi.org/10.1093/nar/gkv416
Ballén-Taborda C, Plata G, Ayling S et al (2013) Identification of cassava MicroRNAs under abiotic stress. Int J Genom 2013:857986. https://doi.org/10.1155/2013/857986
Berka M, Kopecká R, Berková V et al (2022) Regulation of heat shock proteins 70 and their role in plant immunity. J Exp Bot 73:1894–1909. https://doi.org/10.1093/jxb/erab549
Bizabani C, Rogans SJ, Rey MEC (2021) Differential miRNA profiles in South African cassava mosaic virus-infected cassava landraces reveal clues to susceptibility and tolerance to cassava mosaic disease. Virus Res 303:198400. https://doi.org/10.1016/j.virusres.2021.198400
Bredeson JV, Lyons JB, Prochnik SE et al (2016) Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nat Biotechnol 34:562–570. https://doi.org/10.1038/nbt.3535
Ceballos H, Rojanaridpiched C, Phumichai C et al (2020) Excellence in cassava breeding: perspectives for the future. Crop Breed Genet Genom. https://doi.org/10.20900/cbgg20200008
Chan AP, Crabtree J, Zhao Q et al (2010) Draft genome sequence of the oilseed species Ricinus communis. Nat Biotechnol 28:951–956. https://doi.org/10.1038/nbt.1674
Chaudhary R, Baranwal VK, Kumar R et al (2019) Genome-wide identification and expression analysis of Hsp70, Hsp90, and Hsp100 heat shock protein genes in barley under stress conditions and reproductive development. Funct Integr Genom 19:1007–1022. https://doi.org/10.1007/s10142-019-00695-y
Chen X, Xia J, Xia Z et al (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 15:33. https://doi.org/10.1186/s12870-014-0355-7
Chen J, Gao T, Wan S et al (2018) Genome-wide identification, classification and expression analysis of the HSP gene superfamily in tea plant (Camellia sinensis). Int J Mol Sci 19:2633. https://doi.org/10.3390/ijms19092633
Chen C, Chen H, Zhang Y et al (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Cho EK, Choi YJ (2009) A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants. Biotechnol Lett 31:597–606. https://doi.org/10.1007/s10529-008-9880-5
Choudhury S, Mansi, Muthusamy SK et al (2021) Genome-wide identification of Ran GTPase family genes from wheat (T. aestivum) and their expression profile during developmental stages and abiotic stress conditions. Funct Integr Genom 21:239–250. https://doi.org/10.1007/s10142-021-00773-0
Cohn M, Bart RS, Shybut M et al (2014) Xanthomonas axonopodis virulence is promoted by a transcription activator-like effector-mediated induction of a SWEET sugar transporter in cassava. Mol Plant-Microbe Interact MPMI 27:1186–1198. https://doi.org/10.1094/MPMI-06-14-0161-R
Dai X, Zhuang Z, Zhao PX (2018) psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Res 46:W49–W54. https://doi.org/10.1093/nar/gky316
Davoudi M, Chen J, Lou Q (2022) Genome-wide identification and expression analysis of Heat Shock Protein 70 (HSP70) gene family in pumpkin (Cucurbita moschata) rootstock under drought stress suggested the potential role of these chaperones in stress tolerance. Int J Mol Sci 23:1918. https://doi.org/10.3390/ijms23031918
Fathima AA, Sanitha M, Tripathi L, Muiruri S (2023) Cassava (Manihot esculenta) dual use for food and bioenergy: a review. Food Energy Secur 12:e380. https://doi.org/10.1002/fes3.380
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29-37. https://doi.org/10.1093/nar/gkr367
Gkanogiannis A, Dereeper A, Szurek B et al (2018) The cassava genome hub [C20]. In: Proc. plant anim. genome XXVI conf. https://agritrop.cirad.fr/587274/. Accessed 3 Feb 2020
Goodstein DM, Shu S, Howson R et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178-1186. https://doi.org/10.1093/nar/gkr944
Horton P, Park K-J, Obayashi T et al (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587. https://doi.org/10.1093/nar/gkm259
Hu C, Lin S, Chi W, Charng Y (2012) Recent gene duplication and subfunctionalization produced a mitochondrial GrpE, the nucleotide exchange factor of the Hsp70 complex, specialized in thermotolerance to chronic heat stress in Arabidopsis. Plant Physiol 158:747–758. https://doi.org/10.1104/pp.111.187674
Jagannadham PTK, Muthusamy SK, Chidambaranathan P (2019) Micromics: a novel approach to understand the molecular mechanisms in plant stress tolerance. In: Wani SH (ed) Recent approaches in omics for plant resilience to climate change. Springer International Publishing, Cham, pp 93–108
Jung K-H, Gho H-J, Nguyen MX et al (2013) Genome-wide expression analysis of HSP70 family genes in rice and identification of a cytosolic HSP70 gene highly induced under heat stress. Funct Integr Genom 13:391–402. https://doi.org/10.1007/s10142-013-0331-6
Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev Mol Cell Biol 11:579–592. https://doi.org/10.1038/nrm2941
Katiyar A, Smita S, Muthusamy SK et al (2015) Identification of novel drought-responsive microRNAs and trans-acting siRNAs from Sorghum bicolor (L.) Moench by high-throughput sequencing analysis. Front Plant Sci 6:506. https://doi.org/10.3389/fpls.2015.00506
Kelley LA, Mezulis S, Yates CM et al (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858. https://doi.org/10.1038/nprot.2015.053
Khatabi B, Arikit S, Xia R et al (2016) High-resolution identification and abundance profiling of cassava (Manihot esculenta Crantz) microRNAs. BMC Genom 17:85. https://doi.org/10.1186/s12864-016-2391-1
Kim S-R, An G (2013) Rice chloroplast-localized heat shock protein 70, OsHsp70CP1, is essential for chloroplast development under high-temperature conditions. J Plant Physiol 170:854–863. https://doi.org/10.1016/j.jplph.2013.01.006
Kohler V, Andréasson C (2020) Hsp70-mediated quality control: should I stay or should I go? Biol Chem 401:1233–1248. https://doi.org/10.1515/hsz-2020-0187
Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Kushawaha AK, Khan A, Sopory SK, Sanan-Mishra N (2021) Priming by high temperature stress induces microrna regulated heat shock modules indicating their involvement in thermopriming response in rice. Life Basel Switz 11:291. https://doi.org/10.3390/life11040291
Landi S, Capasso G, Ben Azaiez FE et al (2019) Different roles of heat shock proteins (70 kDa) during abiotic stresses in barley (Hordeum vulgare) genotypes. Plants 8:248. https://doi.org/10.3390/plants8080248
Leng L, Liang Q, Jiang J et al (2017) A subclass of HSP70s regulate development and abiotic stress responses in Arabidopsis thaliana. J Plant Res 130:349–363. https://doi.org/10.1007/s10265-016-0900-6
Lescot M, Déhais P, Thijs G et al (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 30:325–327. https://doi.org/10.1093/nar/30.1.325
Letunic I, Khedkar S, Bork P (2021) SMART: recent updates, new developments and status in 2020. Nucleic Acids Res 49:D458–D460. https://doi.org/10.1093/nar/gkaa937
Lu Y, Zhao P, Zhang A et al (2022) Genome-wide analysis of HSP70s in hexaploid wheat: tandem duplication, heat response, and regulation. Cells 11:818. https://doi.org/10.3390/cells11050818
Luo S, Ma Q, Zhong Y et al (2022) Editing of the starch branching enzyme gene SBE2 generates high-amylose storage roots in cassava. Plant Mol Biol 108:429–442. https://doi.org/10.1007/s11103-021-01215-y
Lyons JB, Bredeson JV, Mansfeld BN et al (2022) Correction to: current status and impending progress for cassava structural genomics. Plant Mol Biol 109:193. https://doi.org/10.1007/s11103-021-01139-7
Maruthi MN, Bouvaine S, Tufan HA et al (2014) Transcriptional response of virus-infected cassava and identification of putative sources of resistance for cassava brown streak disease. PLoS ONE 9:e96642. https://doi.org/10.1371/journal.pone.0096642
Masand S, Yadav SK (2016) Overexpression of MuHSP70 gene from Macrotyloma uniflorum confers multiple abiotic stress tolerance in transgenic Arabidopsis thaliana. Mol Biol Rep 43:53–64. https://doi.org/10.1007/s11033-015-3938-y
Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci CMLS 62:670–684. https://doi.org/10.1007/s00018-004-4464-6
Morgan NK, Choct M (2016) Cassava: Nutrient composition and nutritive value in poultry diets. Anim Nutr 2:253–261. https://doi.org/10.1016/j.aninu.2016.08.010
Muñoz-Bodnar A, Perez-Quintero AL, Gomez-Cano F et al (2014) RNAseq analysis of cassava reveals similar plant responses upon infection with pathogenic and non-pathogenic strains of Xanthomonas axonopodis pv. manihotis. Plant Cell Rep 33:1901–1912. https://doi.org/10.1007/s00299-014-1667-7
Muthusamy SK, Dalal M, Chinnusamy V, Bansal KC (2016) Differential regulation of genes coding for organelle and cytosolic ClpATPases under biotic and abiotic stresses in wheat. Front Plant Sci 7:929. https://doi.org/10.3389/fpls.2016.00929
Muthusamy SK, Dalal M, Chinnusamy V, Bansal KC (2017) Genome-wide identification and analysis of biotic and abiotic stress regulation of small heat shock protein (HSP20) family genes in bread wheat. J Plant Physiol 211:100–113. https://doi.org/10.1016/j.jplph.2017.01.004
Muthusamy SK, Amina AT, Hegde V et al (2019) Comprehensive analysis of MeGRAS Family genes in cassava and their genome collinearity relationship with Arabidopsis and Populus genome. J Root Crops 45:3–11
Ni Z, Liu N, Yu Y et al (2021) The cotton 70-kDa heat shock protein GhHSP70–26 plays a positive role in the drought stress response. Environ Exp Bot 191:104628. https://doi.org/10.1016/j.envexpbot.2021.104628
Otun S, Escrich A, Achilonu I et al (2022) The future of cassava in the era of biotechnology in Southern Africa. Crit Rev Biotechnol. https://doi.org/10.1080/07388551.2022.2048791
Panzade KP, Kale SS, Chavan NR, Hatzade B (2021) Genome-wide analysis of Hsp70 and Hsp100 gene families in Ziziphus jujuba. Cell Stress Chaperones 26:341–353. https://doi.org/10.1007/s12192-020-01179-w
Pérez-Quintero ÁL, Quintero A, Urrego O et al (2012) Bioinformatic identification of cassava miRNAs differentially expressed in response to infection by Xanthomonas axonopodis pv. manihotis. BMC Plant Biol 12:29. https://doi.org/10.1186/1471-2229-12-29
Reynolds CR, Islam SA, Sternberg MJE (2018) EzMol: a web server wizard for the rapid visualization and image production of protein and nucleic acid structures. J Mol Biol 430:2244–2248. https://doi.org/10.1016/j.jmb.2018.01.013
Rogans SJ, Rey C (2016) Unveiling the micronome of cassava (Manihot esculenta Crantz). PLoS ONE 11:e0147251. https://doi.org/10.1371/journal.pone.0147251
Rosenzweig R, Nillegoda NB, Mayer MP, Bukau B (2019) The Hsp70 chaperone network. Nat Rev Mol Cell Biol 20:665–680. https://doi.org/10.1038/s41580-019-0133-3
Rowarth NM, Dauphinee AN, Denbigh GL, Gunawardena AH (2020) Hsp70 plays a role in programmed cell death during the remodelling of leaves of the lace plant (Aponogeton madagascariensis). J Exp Bot 71:907–918. https://doi.org/10.1093/jxb/erz447
Sarkar NK, Kundnani P, Grover A (2013) Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress Chaperones 18:427–437. https://doi.org/10.1007/s12192-012-0395-6
Sievers F, Higgins DG (2018) Clustal Omega for making accurate alignments of many protein sequences. Protein Sci Publ Protein Soc 27:135–145. https://doi.org/10.1002/pro.3290
Singh G, Sarkar NK, Grover A (2021) Hsp70, sHsps and ubiquitin proteins modulate HsfA6a-mediated Hsp101 transcript expression in rice (Oryza sativa L.). Physiol Plant 173:2055–2067. https://doi.org/10.1111/ppl.13552
Sivan S, Arya K, Sheela MN et al (2023) Genetic diversity analysis of Indian Cassava (Manihot esculenta Crantz) accessions using morphological and molecular markers. South Afr J Bot 161:347–357. https://doi.org/10.1016/j.sajb.2023.08.027
Su P-H, Li H (2010) Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. Plant Cell 22:1516–1531. https://doi.org/10.1105/tpc.109.071415
Su H, Xing M, Liu X et al (2019) Genome-wide analysis of HSP70 family genes in cabbage (Brassica oleracea var. capitata) reveals their involvement in floral development. BMC Genom 20:369. https://doi.org/10.1186/s12864-019-5757-3
Sung DY, Vierling E, Guy CL (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol 126:789–800. https://doi.org/10.1104/pp.126.2.789
Tabassum R, Dosaka T, Ichida H et al (2020) FLOURY ENDOSPERM11-2 encodes plastid HSP70-2 involved with the temperature-dependent chalkiness of rice (Oryza sativa L.) grains. Plant J Cell Mol Biol 103:604–616. https://doi.org/10.1111/tpj.14752
Tabusam J, Shi Q, Feng D et al (2022) HSP70 Gene Family in Brassica rapa: genome-wide identification, characterization, and expression patterns in response to heat and cold stress. Cells 11:2316. https://doi.org/10.3390/cells11152316
Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604. https://doi.org/10.1126/science.1128691
Usman MG, Rafii MY, Martini MY et al (2017) Molecular analysis of Hsp70 mechanisms in plants and their function in response to stress. Biotechnol Genet Eng Rev 33:26–39. https://doi.org/10.1080/02648725.2017.1340546
Velankar S, Burley SK, Kurisu G et al (2021) The protein data bank archive. Methods Mol Biol Clifton NJ 2305:3–21. https://doi.org/10.1007/978-1-0716-1406-8_1
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. https://doi.org/10.1093/jhered/93.1.77
Vu NT, Kamiya K, Fukushima A et al (2019) Comparative co-expression network analysis extracts the SlHSP70 gene affecting to shoot elongation of tomato. Plant Biotechnol 36:143–153. https://doi.org/10.5511/plantbiotechnology.19.0603a
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:e49. https://doi.org/10.1093/nar/gkr1293
Wang RY-R, Noddings CM, Kirschke E et al (2022) Structure of Hsp90-Hsp70-Hop-GR reveals the Hsp90 client-loading mechanism. Nature 601:460–464. https://doi.org/10.1038/s41586-021-04252-1
Waters ER, Vierling E (2020) Plant small heat shock proteins—evolutionary and functional diversity. New Phytol 227:24–37. https://doi.org/10.1111/nph.16536
Wei S-S, Niu W-T, Zhai X-T et al (2019) Arabidopsis mtHSC70-1 plays important roles in the establishment of COX-dependent respiration and redox homeostasis. J Exp Bot 70:5575–5590. https://doi.org/10.1093/jxb/erz357
Wen F, Wu X, Li T et al (2017) Genome-wide survey of heat shock factors and heat shock protein 70s and their regulatory network under abiotic stresses in Brachypodium distachyon. PLoS ONE 12:e0180352. https://doi.org/10.1371/journal.pone.0180352
Wilson MC, Mutka AM, Hummel AW et al (2017) Gene expression atlas for the food security crop cassava. New Phytol 213:1632–1641. https://doi.org/10.1111/nph.14443
Yang M, Derbyshire MK, Yamashita RA, Marchler-Bauer A (2020) NCBI’s conserved domain database and tools for protein domain analysis. Curr Protoc Bioinforma 69:e90. https://doi.org/10.1002/cpbi.90
Yer EN, Baloglu MC, Ziplar UT et al (2016) Drought-responsive Hsp70 gene analysis in populus at genome-wide level. Plant Mol Biol Report 34:483–500. https://doi.org/10.1007/s11105-015-0933-3
Yu A, Li P, Tang T et al (2015) Roles of Hsp70s in stress responses of microorganisms, plants, and animals. BioMed Res Int 2015:510319. https://doi.org/10.1155/2015/510319
Zeng C, Ding Z, Zhou F et al (2017a) The discrepant and similar responses of genome-wide transcriptional profiles between drought and cold stresses in cassava. Int J Mol Sci 18:2668. https://doi.org/10.3390/ijms18122668
Zeng C, Xia J, Chen X et al (2017b) MicroRNA-like RNAs from the same miRNA precursors play a role in cassava chilling responses. Sci Rep 7:17135. https://doi.org/10.1038/s41598-017-16861-w
Zhai X-T, Wei S-S, Liang W-Q et al (2020) Arabidopsis mtHSC70-1 physically interacts with the Cox2 subunit of cytochrome c oxidase. Plant Signal Behav 15:1714189. https://doi.org/10.1080/15592324.2020.1714189
Zhang Q, Kong X, Yu Q et al (2019) Responses of PYR/PYL/RCAR ABA receptors to contrasting stresses, heat and cold in Arabidopsis. Plant Signal Behav 14:1670596. https://doi.org/10.1080/15592324.2019.1670596
Zhao D, Xia X, Su J et al (2019) Overexpression of herbaceous peony HSP70 confers high temperature tolerance. BMC Genom 20:70. https://doi.org/10.1186/s12864-019-5448-0
Zhou R, Macaya-Sanz D, Carlson CH et al (2020) A willow sex chromosome reveals convergent evolution of complex palindromic repeats. Genome Biol 21:38. https://doi.org/10.1186/s13059-020-1952-4
Zuiderweg ERP, Hightower LE, Gestwicki JE (2017) The remarkable multivalency of the Hsp70 chaperones. Cell Stress Chaperones 22:173–189. https://doi.org/10.1007/s12192-017-0776-y
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they do not have competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Muthusamy, S.K., Pushpitha, P., Makeshkumar, T. et al. Genome-wide identification and expression analysis of Hsp70 family genes in Cassava (Manihot esculenta Crantz). 3 Biotech 13, 341 (2023). https://doi.org/10.1007/s13205-023-03760-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-023-03760-3