Log in

Genome-wide identification and characterization of filamentation temperature-sensitive H (FtsH) genes and expression analysis in response to multiple stresses in Medicago truncatula

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

Filamentation temperature-sensitive H (FtsH) is an AAA+ ATP-dependent protease that plays a vital role in plant environmental adaption and tolerance. However, little is known about the function of the FtsH gene family in the most important legume model plant, Medicago truncatula.

Methods and results

To identify and investigate the potential stress adaptation roles of FtsH gene family in M. truncatula, we conducted a series of genome-wide characterization and expression analyses. Totally, twenty MtFtsH genes were identified, which were unevenly distributed across eight chromosomes and classified into six evolution groups based on their phylogenetic relationships, with each group containing similar structures and motifs. Furthermore, MtFtsH genes exhibited a high degree of collinearity and homology with leguminous plants such as alfalfa and soybean. Multiple cis-elements in the upstream region of MtFtsH genes were also identified that responded to light, abiotic stress, and phytohormones. Public RNA-seq data indicated that MtFtsH genes were induced under both salt and drought stresses, and our transcript expression analysis showed that MtFtsH genes of MtFtsH1, MtFtsH2, MtFtsH4, MtFtsH9, and MtFtsH10 were up-regulated after ABA, H2O2, PEG, and NaCl treatments. These results suggest that MtFtsH genes may play a critical role in drought and high salt stress responses and the adaption processes of plants.

Conclusions

This study provides a systematic analysis of FtsH gene family in M. truncatula, serving as a valuable molecular theoretical basis for future functional investigations. Our findings also extend the pool of potential candidate genes for the genetic improvement of abiotic stress tolerance in legume crops.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The transcriptome sequencing (RNA-seq) data obtained from Medicago truncatula Gene Expression Atlas database and are available at the following URL: https://medicago.toulouse.inrae.fr/GEA. Examples from https://pubmed.ncbi.nlm.nih.gov/24661137/ and https://pubmed.ncbi.nlm.nih.gov/31505820/.

References

  1. Klaus Leonhard JMH, Stuart RA, Walter Neupert GM, Langer T (1996) AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. The EMBO J 15:4218–4229

    Article  Google Scholar 

  2. Szymon K, Andrzej MB, Chandra V, Kiyonobu K, Anthony JW (2002) The crystal structure of the AAA domain of the ATP-dependent protease FtsH of Escherichia coli at 1.5 Å resolution. Elsevier Sci Ltd 10:1073–1083

    Google Scholar 

  3. Wagner R, Aigner H, Funk C (2012) FtsH proteases located in the plant chloroplast. Physiol Plant 145:203–214. https://doi.org/10.1111/j.1399-3054.2011.01548.x

    Article  CAS  PubMed  Google Scholar 

  4. Klaus Leonhard JMH, Stuart RA, Walter Neupert GM, Langer T (1996) AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. The EMBO J 15:4218–4229

    Article  Google Scholar 

  5. Tomoyasu T, Yamanaka K, Murata K, Suzaki T, Bouloc P, Kato A (1993) Topology and subcellular localization of FtsH protein in Escherichia coli. J Bacteriol 175:1352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Elke Deuerling BP, Schumann W (1995) The ftsH gene of Bacillus subtilis is transiently induced after osmotic and temperature upshift. J Bacteriol 177:4105–4112

    Article  Google Scholar 

  7. Beier D, Spohn G, Rappuoli R, Scarlato V (1997) Identification and characterization of an operon of Helicobacter pylori that is involved in motility and stress adaptation. J Bacteriol 179:4676–4683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Garcia-Lorenzo M, Sjodin A, Jansson S, Funk C (2006) Protease gene families in populus and Arabidopsis. BMC Plant Biol 6:30. https://doi.org/10.1186/1471-2229-6-30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zhang J, Sun A (2009) Genome-wide comparative analysis of the metalloprotease ftsH gene families between Arabidopsis thaliana and rice. J Biotechnol 25(29):1402–1408

    CAS  Google Scholar 

  10. Ivashuta S, Imai R, Uchiyama K, Gau M, Shimamoto Y (2002) Changes in chloroplast FtsH-like gene during cold acclimation in alfalfa (Medicago sativa). J Plant Physiol 159:85–90. https://doi.org/10.1078/0176-1617-00661

    Article  CAS  Google Scholar 

  11. Yin Z, Meng F, Song H, Wang X, Chao M, Zhang G, Xu X, Deng D, Yu D (2011) GmFtsH9 expression correlates with in vivo photosystem II function: chlorophyll a fluorescence transient analysis and eQTL map** in soybean. Planta 234:815–827. https://doi.org/10.1007/s00425-011-1445-5

    Article  CAS  PubMed  Google Scholar 

  12. Liu Q, Galli M, Liu X, Federici S, Buck A, Cody J, Labra M, Gallavotti A (2019) NEEDLE1 encodes a mitochondria localized ATP-dependent metalloprotease required for thermotolerant maize growth. PANS 116:19736–19742. https://doi.org/10.1073/pnas.1907071116

    Article  CAS  Google Scholar 

  13. Xu K, Song J, Wu Y, Zhuo C, Wen J, Yi B, Ma C, Shen J, Fu T, Tu J (2022) Brassica evolution of essential BnaFtsH1 genes involved in the PSII repair cycle and loss of FtsH5. Plant Sci 315:111128. https://doi.org/10.1016/j.plantsci.2021.111128

    Article  CAS  PubMed  Google Scholar 

  14. Ferro M, Brugiere S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, Ramus C, Miras S, Mellal M, Le Gall S et al (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 9:1063–1084. https://doi.org/10.1074/mcp.M900325-MCP200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Janska H (2005) ATP-dependent proteases in plant mitochondria: what do we know about them today? Physiol Plant 123:399–405. https://doi.org/10.1111/j.1399-3054.2004.00439.x

    Article  CAS  Google Scholar 

  16. Sun JL, Li JY, Wang MJ, Song ZT, Liu JX (2021) Protein quality control in plant organelles: current progress and future perspectives. Mol Plant 14:95–114. https://doi.org/10.1016/j.molp.2020.10.011

    Article  CAS  PubMed  Google Scholar 

  17. Yu F, Park S, Rodermel SR (2005) Functional redundancy of AtFtsH metalloproteases in thylakoid membrane complexes. Plant Physiol 138:1957–1966. https://doi.org/10.1104/pp.105.061234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kikuchi S, Asakura Y, Imai M, Nakahira Y, Kotani Y, Hashiguchi Y, Nakai Y, Takafuji K, Bedard J, Hirabayashi-Ishioka Y et al (2018) A Ycf2-FtsHi heteromeric AAA-ATPase complex is required for chloroplast protein import. Plant Cell 30:2677–2703. https://doi.org/10.1105/tpc.18.00357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Mishra LS, Mishra S, Caddell DF, Coleman-Derr D, Funk C (2021) The plastid-localized AtFtsHi3 pseudo-protease of Arabidopsis thaliana has an impact on plant growth and drought tolerance. Front Plant Sci 12:694727. https://doi.org/10.3389/fpls.2021.694727

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ivanova A, Ghifari AS, Berkowitz O, Whelan J, Murcha MW (2021) The mitochondrial AAA protease FTSH3 regulates complex I abundance by promoting its disassembly. Plant Physiol 186:599–610. https://doi.org/10.1093/plphys/kiab074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Sedaghatmehr M, Thirumalaikumar VP, Kamranfar I, Schulz K, Mueller-Roeber B, Sampathkumar A, Balazadeh S (2021) Autophagy complements metalloprotease FtsH6 in degrading plastid heat shock protein HSP21 during heat stress recovery. J Exp Bot. https://doi.org/10.1093/jxb/erab304

    Article  PubMed  Google Scholar 

  22. Maziak A, Heidorn-Czarna M, Weremczuk A, Janska H (2021) FTSH4 and OMA1 mitochondrial proteases reduce moderate heat stress-induced protein aggregation. Plant Physiol 187:769–786. https://doi.org/10.1093/plphys/kiab296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Qianwen Y, Mingna L, Ruicai L, Qingchuan Y, Junmei K, Changhong G (2021) Cloning and functional analysis of MsFtsH8 gene from Medicago sativa. J Plant Genet Resour. https://doi.org/10.13430/j.cnki.jpgr.20210309001

    Article  Google Scholar 

  24. Chen J, Burke JJ, Velten J, **n Z (2006) FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J 48:73–84. https://doi.org/10.1111/j.1365-313X.2006.02855.x

    Article  CAS  PubMed  Google Scholar 

  25. Cook DR (1999) Medicago truncatula—a model in the making!: commentary. Curr Opin Plant Biol 2:301–304. https://doi.org/10.1016/S1369-5266(99)80053-3

    Article  CAS  PubMed  Google Scholar 

  26. Li M, Yu A, Sun Y, Hu Q, Kang J, Chen L, Zhu X, Yang Q, Long R (2023) Lipid composition remodeling and storage lipid conversion play a critical role in salt tolerance in alfalfa (Medicago sativa L.) leaves. Environ Exp Bot 205:105144. https://doi.org/10.1016/j.envexpbot.2022.105144

    Article  CAS  Google Scholar 

  27. Guo Z, Gao X, Cai H, Yu L, Gu C, Zhang SL (2021) Genome-wide identification, evolution and expression analysis of the FtsH gene during fruit development in pear (Pyrus bretschneideri). Plant Biotechnol Rep 15:537–550. https://doi.org/10.1007/s11816-021-00686-1

    Article  CAS  Google Scholar 

  28. Pu T, Mo Z, Su L, Yang J, Wan K, Wang L, Liu R, Liu Y (2022) Genome-wide identification and expression analysis of the ftsH protein family and its response to abiotic stress in Nicotiana tabacum L. BMC Genomics 23:503. https://doi.org/10.1186/s12864-022-08719-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, **a R (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

    Article  CAS  PubMed  Google Scholar 

  30. Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL, Tosatto SCE, Paladin L, Raj S, Richardson LJ (2021) Pfam: the protein families database in 2021. Nucleic Acids Res. https://doi.org/10.1093/nar/gkaa913

    Article  PubMed  Google Scholar 

  31. Madeira F, Pearce M, Tivey ARN, Basutkar P, Lee J, Edbali O, Madhusoodanan N, Kolesnikov A, Lopez R (2022) Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res. https://doi.org/10.1093/nar/gkac240

    Article  PubMed  PubMed Central  Google Scholar 

  32. Carrere S, Verdier J, Gamas P (2021) MtExpress, a comprehensive and curated RNAseq-based gene expression atlas for the model legume Medicago truncatula. Plant Cell Physiol 62:1494–1500. https://doi.org/10.1093/pcp/pcab110

    Article  CAS  PubMed  Google Scholar 

  33. Hu B, Wu H, Huang W, Song J, Zhou Y, Lin Y (2019) SWEET gene family in Medicago truncatula: genome-wide identification, expression and substrate specificity analysis. Plants. https://doi.org/10.3390/plants8090338

    Article  PubMed  PubMed Central  Google Scholar 

  34. Zhang JY, Cruz De Carvalho MH, Torres-Jerez I, Kang YUN, Allen SN, Huhman DV, Tang Y, Murray J, Sumner LW, Udvardi MK (2014) Global reprogramming of transcription and metabolism in Medicago truncatula during progressive drought and after rewatering. Plant Cell Environ 37:2553–2576. https://doi.org/10.1111/pce.12328

    Article  PubMed  PubMed Central  Google Scholar 

  35. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  36. Roy SW, Penny D (2007) A very high fraction of unique intron positions in the intron-rich diatom Thalassiosira pseudonana indicates widespread intron gain. Mol Biol Evol 24:1447–1457. https://doi.org/10.1093/molbev/msm048

    Article  CAS  PubMed  Google Scholar 

  37. Yue G, Hu X, He Y, Yang A, Zhang J (2010) Identification and characterization of two members of the FtsH gene family in maize (Zea mays L.). Mol Biol Rep 37:855–863. https://doi.org/10.1007/s11033-009-9691-3

    Article  CAS  PubMed  Google Scholar 

  38. **ong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165-183. https://doi.org/10.1105/tpc.000596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Li M, Zhang K, Sun Y, Cui H, Cao S, Yan L, Xu M (2018) Growth, physiology, and transcriptional analysis of Two contrasting Carex rigescens genotypes under Salt stress reveals salt-tolerance mechanisms. J Plant Physiol 229:77–88. https://doi.org/10.1016/j.jplph.2018.07.005

    Article  CAS  PubMed  Google Scholar 

  40. Das A, Eldakak M, Paudel B, Kim DW, Hemmati H, Basu C, Rohila JS (2016) Leaf proteome analysis reveals prospective drought and heat stress response mechanisms in soybean. Biomed Res Int 2016:6021047. https://doi.org/10.1155/2016/6021047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Dolzblasz A, Smakowska E, Gola EM, Sokolowska K, Kicia M, Janska H (2016) The mitochondrial protease AtFTSH4 safeguards Arabidopsis shoot apical meristem function. Sci Rep 6:28315. https://doi.org/10.1038/srep28315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Smakowska E, Skibior-Blaszczyk R, Czarna M, Kolodziejczak M, Kwasniak-Owczarek M, Parys K, Funk C, Janska H (2016) Lack of FTSH4 protease affects protein carbonylation, mitochondrial morphology, and phospholipid content in mitochondria of arabidopsis: new insights into a complex interplay. Plant Physiol 171:2516–2535. https://doi.org/10.1104/pp.16.00370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wang L, Kim C, Xu X, Piskurewicz U, Dogra V, Singh S, Mahler H, Apel K (2016) Singlet oxygen- and EXECUTER1-mediated signaling is initiated in grana margins and depends on the protease FtsH2. PNAS 113:E3792-3800. https://doi.org/10.1073/pnas.1603562113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Tian YN, Zhong RH, Wei JB, Luo HH, Eyal Y, ** HL, Wu LJ, Liang KY, Li YM, Chen SZ et al (2021) Arabidopsis CHLOROPHYLLASE 1 protects young leaves from long-term photodamage by facilitating FtsH-mediated D1 degradation in photosystem II repair. Mol Plant 14:1149–1167. https://doi.org/10.1016/j.molp.2021.04.006

    Article  CAS  PubMed  Google Scholar 

  45. Kato Y, Miura E, Ido K, Ifuku K, Sakamoto W (2009) The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. Plant Physiol 151:1790–1801. https://doi.org/10.1104/pp.109.146589

    Article  PubMed  PubMed Central  Google Scholar 

  46. Andersson FI, Tryggvesson A, Sharon M, Diemand AV, Classen M, Best C, Schmidt R, Schelin J, Stanne TM, Bukau B (2009) Structure and function of a novel type of ATP-dependent Clp protease. J Biol Chem 284:13519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Schreier TB, Clery A, Schlafli M, Galbier F, Stadler M, Demarsy E, Albertini D, Maier BA, Kessler F, Hortensteiner S et al (2018) Plastidial NAD-dependent malate dehydrogenase: a moonlighting protein involved in early chloroplast development through its interaction with an FtsH12-FtsHi protease complex. Plant Cell 30:1745–1769. https://doi.org/10.1105/tpc.18.00121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Mishra LS, Mielke K, Wagner R, Funk C (2019) Reduced expression of the proteolytically inactive FtsH members has impacts on the Darwinian fitness of Arabidopsis thaliana. J Exp Bot 70:2173–2184. https://doi.org/10.1093/jxb/erz004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 32101421), Key project of science and technology vitalize Mongolia action (Grant No. NMKJXM202110-5), Agricultural Science and Technology Innovation Program, China (ASTIP-IAS14), China Agriculture Research System of MOF, and MARA, China (CARS-34), the National Natural Science Foundation of China (Grant No. U21A20182).

Author information

Authors and Affiliations

Authors

Contributions

XZ and ML conceived and designed the experiments; XZ, AY, and YZ conducted the genomic identification and characterization analysis of the gene family; XZ and QY prepared the plant materials and performed the qRT-PCR experiment; XZ and ML completed the figures; XZ and ML wrote the manuscript; and XZ, JK, QY, CG, and ML revised and finalized the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Changhong Guo or Mingna Li.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 49 KB)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, X., Yu, A., Zhang, Y. et al. Genome-wide identification and characterization of filamentation temperature-sensitive H (FtsH) genes and expression analysis in response to multiple stresses in Medicago truncatula. Mol Biol Rep 50, 10097–10109 (2023). https://doi.org/10.1007/s11033-023-08851-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-023-08851-1

Keywords

Navigation