Abstract
Biotic and abiotic stresses are among major factors limiting crop yields, and Filamentation temperature-sensitive (FtsH) genes are one of the key regulators of plant response to these stresses. The FtsH is an ATP-dependent metalloprotease in prokaryotes and eukaryotes. Due to the economic importance and cultivation of potato grown in the biotic and abiotic stress prone areas, identification and characterization of FtsH family members are crucially important. The present research was conducted to investigate FtsH family members in potato under stressful regime. To detect the FtsH genes in potato, we performed genome-wide analysis of FtsH genes in the Solanum tuberosum genome using the Ensemble Plant. All putative sequences were approved with the Pfam. Bioinformatics analysis was conducted using phylogenetic tree, gene structure, Transcription factor-binding site (TFBS) analysis, protein–protein interaction, and gene expression. The members of FtsH were categorized into eight groups. Some of the FtsH proteins were subcellularly located in the nucleus and chloroplast. The number of introns was ranged from 3 to 14 in gene family members. Totally, 33 TFBS including biotic and abiotic stress-responsive elements were found in FtsH promoter sequences. MYB and WRKY were the highest number among TFBS which were involved in abiotic and biotic stresses. Gene expression analysis revealed that the StFtsH2 and StFtsH5 had the highest gene expression, induced by abiotic and biotic stresses in all three tissues of stem, root, and leaves. It is expected that the StFtsH2 and StFtsH5 could be used in plant manipulation and breeding programs aimed for tolerance enhancement to abiotic (cold, heat, and high light) and biotic stresses [Potato virus Y (PVY), Potato virus X (PVX), Potato virus A (PVA), Potato virus X (PVA), and Potato virus S (PVS)].
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Abbreviations
- AP2:
-
APETALA2
- ATH:
-
AT hook
- B3:
-
B3 DNA-binding domain (DBD)
- bHLH:
-
Basic Helix–Loop–Helix
- bZIP:
-
Basic Leucine Zipper
- C2H2 ZF:
-
Cchhc domain of neural zinc finger factor
- CSD:
-
Cold shock domain
- Dof:
-
Dof (DNA binding with one finger) domain
- EIN3:
-
Ethylene insensitive 3
- FAR1:
-
FAR domain (Finger-Associated Repeats)
- GATA:
-
GATA-binding factors
- HB:
-
Homeodomain
- LOB:
-
Lateral organ boundaries
- MADS box:
-
The conserved domain originally discovered in four genes (MCM1, AG, DEF A, and SRF)
- Myb:
-
Myeloblastosis
- NAC:
-
No apical meristem [NAM], Arabidopsis transcription activation factor [ATAF], and cup-shaped cotyledon [CUC])-domain transcription factor gene
- SBP:
-
SQUAMOSA-pROMOTER-BINDING PROTEIN
- STK:
-
Storekeeper
- TCP:
-
Teosinte branched 1 (tb1, Zea mays (Maize)), cycloidea (cyc) (Antirrhinum majus) (Garden snapdragon) and PCF in rice (Oryza sativa)
- WRKY:
-
WRKY transcription factor family
- ZF-HD:
-
Zinc finger homeodomain
- Trihelix:
-
Helix–loop–helix–loop–helix
- SRS:
-
SHORT INTERNODES-related sequence
- SOX:
-
SRY-related high-mobility group box
- WRC:
-
Trp-Arg-Cys
- WOX:
-
WUSCHEL-related homeobox
- BES1:
-
BRI1-EMSSUPPRESSOR1
- VOZ:
-
VASCULAR PLANT ONE-ZINC FINGER
- NF-YB:
-
Nuclear Transcription Factor Y Subunit Beta
- TCR:
-
Transcription-coupled repeat
- MADF:
-
Mothers against Dpp factor
- ARF:
-
Auxin-responsive element
- HSF:
-
Heat Shock Factor
- HD-ZIP:
-
Homeodomain-leucine zipper
References
Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15(12):664–674
Ali M, Baek KH (2020) Protective roles of cytosolic and plastidal proteasomes on abiotic stress and pathogen invasion. Plants 9(7):832
Arefian M, Vessal S, Malekzadeh-Shafaroudi S, Siddique KH, Bagheri A (2019) Comparative proteomics and gene expression analyses revealed responsive proteins and mechanisms for salt tolerance in chickpea genotypes. BMC Plant Biol 19(1):1–26
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202-208
Chang WC, Lee TY, Huang HD, Huang HY, Pan RL (2008) PlantPAN: plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genom 9(1):1–4
Chen J, Burke JJ, Velten J, Xin Z (2006) FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J 48(1):73–84
Desclos M, Etienne P, Coquet L, Jouenne T, Bonnefoy J, Segura R, Reze S, Ourry A, Avice JC (2009) A combined 15N tracing/proteomics study in Brassica napus reveals the chronology of proteomics events associated with N remobilisation during leaf senescence induced by nitrate limitation or starvation. Proteomics 9(13):3580–3608
Gibala M, Kicia M, Sakamoto W, Gola EM, Kubrakiewicz J, Smakowska E, Janska H (2009) The lack of mitochondrial AtFtsH4 protease alters Arabidopsis leaf morphology at the late stage of rosette development under short-day photoperiod. Plant J 59(5):685–699
Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Hereditas 29(8):1023–1026
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(4):537–550
Gururani MA, Venkatesh J, Tran LS (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8(9):1304–1320
Hajibarat Z, Saidi A, Zeinalabedini M, Gorji AM, Ghaffari MR, Shariati V, Ahmadvand R (2022) Genome-wide identification of StU-box gene family and assessment of their expression in developmental stages of Solanum tuberosum. J Genet Eng Biotechnol 20(1):1–21
He GH, Xu JY, Wang YX, Liu JM, Li PS, Chen M, Ma YZ, Xu ZS (2016) Drought-responsive WRKY transcription factor genes TaWRKY1 and TaWRKY33 from wheat confer drought and/or heat resistance in Arabidopsis. BMC Plant Biol 16(1):1–6
Herman C, Thévenet D, D’Ari RI, Bouloc P (1995) Degradation of sigma 32, the heat shock regulator in Escherichia coli, is governed by HflB. PNAS 92(8):3516–3520
Hrmova M, Hussain SS (2021) Plant transcription factors involved in drought and associated stresses. Int J Mol Sci 22(11):5662
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(1):85–90
Johnson SM, Lim FL, Finkler A, Fromm H, Slabas AR, Knight MR (2014) Transcriptomic analysis of sorghum bicolor responding to combined heat and drought stress. BMC Genet 15(1):1–9
Kicia M, Gola EM, Janska H (2010) Mitochondrial protease AtFtsH4 protects ageing Arabidopsis rosettes against oxidative damage under short-day photoperiod. Plant Signal Behav 5(2):126–128
Kihara A, Akiyama Y, Ito K (1997) Host regulation of lysogenic decision in bacteriophage λ: transmembrane modulation of FtsH (HflB), the cII degrading protease, by HflKC (HflA). PNAS 94(11):5544–5549
Kwasniak M, Pogorzelec L, Migdal I, Smakowska E, Janska H (2012) Proteolytic system of plant mitochondria. Physiol Plant 145(1):187–195
Li D, Liu X, Shu L, Zhang H, Zhang S, Song Y, Zhang Z (2020) Global analysis of the AP2/ERF gene family in rose (Rosa chinensis) genome unveils the role of RcERF099 in Botrytis resistance. BMC Plant Biol 20(1):1–5
Li JB, Luan YS, Liu Z (2015) SpWRKY1 mediates resistance to Phytophthora infestans and tolerance to salt and drought stress by modulating reactive oxygen species homeostasis and expression of defense-related genes in tomato. PCTOC 123(1):67–81
Liang L, Chen M, Sun H, Shi Y, Sun B, Li H (2019) Study of the interaction between wheat FtsH2 and wheat yellow mosaic virus CP. Acta Phytophysiol Sin 49(6):799–807
Liu B, Hong YB, Zhang YF, Li XH, Huang L, Zhang HJ, Li DY, Song FM (2014) Tomato WRKY transcriptional factor SlDRW1 is required for disease resistance against Botrytis cinerea and tolerance to oxidative stress. Plant Sci 227:145–156
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408
Lopes KL, Rodrigues RA, Silva MC, Braga WG, Silva-Filho MC (2018) The Zinc-finger thylakoid-membrane protein FIP is involved with abiotic stress response in Arabidopsis thaliana. Front Plant Sci 9:504
Luo P, Li Z, Chen W, Xing W, Yang J, Cui Y (2020) Overexpression of RmICE1, a bHLH transcription factor from Rosa multiflora, enhances cold tolerance via modulating ROS levels and activating the expression of stress-responsive genes. EEB 178:104160
Majsec K, Bhuiyan NH, Sun Q, Kumari S, Kumar V, Ware D, van Wijk KJ (2017) The plastid and mitochondrial peptidase network in Arabidopsis thaliana: a foundation for testing genetic interactions and functions in organellar proteostasis. Plant Cell 29(11):2687–2710
Mishra LS, Funk C (2021) The FtsHi enzymes of Arabidopsis thaliana: pseudo-proteases with an Important function. Int J Mol Sci 22(11):5917
Navabpour S, Morris K, Allen R, Harrison E, Mackerness AHS, Buchanan-Wollaston V (2003) Expression of senescence-enhanced genes in response to oxidative stress. J Exp Bot 54(391):2285–2292
Ogura T, Wilkinson AJ (2001) AAA+ superfamily ATPases: common structure–diverse function. Genes Cells 6(7):575–597
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 Genom 23(1):1–5
Rigas S, Daras G, Laxa M, Marathias N, Fasseas C, Sweetlove LJ, Hatzopoulos P (2009) Role of Lon1 protease in post-germinative growth and maintenance of mitochondrial function in Arabidopsis thaliana. New Phytol 181(3):588–600
Saidi A, Hajibarat Z (2019) Characterization of cis-elements in hormonal stress-responsive genes in Oryza sativa. Asia Pac J Mol Biol Biotechnol 27(1):95–102
Saidi A, Hajibarat Z, Hajibarat Z (2020) Transcriptome analysis of Phytophthora infestans and Colletotrichum coccodes in tomato to reveal resistance mechanisms. Asia Pac J Mol Biol Biotechnol 28(1):39–51
Saidi A, Hajibarat Z, Hajibarat Z (2021) Phylogeny, gene structure and GATA genes expression in different tissues of solanaceae species. Biocatal Agric Biotechnol 35:102015
Sakamoto W, Zaltsman A, Adam Z, Takahashi Y (2003) Coordinated regulation and complex formation of yellow variegated1 and yellow variegated2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell 15(12):2843–2855
Sakuraba Y, Lee SH, Kim YS, Park OK, Hörtensteiner S, Paek NC (2014) Delayed degradation of chlorophylls and photosynthetic proteins in Arabidopsis autophagy mutants during stress-induced leaf yellowing. J Exp Bot 65(14):3915–3925
Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37(5):501–506
Schumann W (1999) FtsH–a single-chain charonin? FEMS Microbiol Rev 23(1):1–1
Sedaghatmehr M, Mueller-Roeber B, Balazadeh S (2016) The plastid metalloprotease FtsH6 and small heat shock protein HSP21 jointly regulate thermomemory in Arabidopsis. Nat Commun 7(1):1–4
Shin R, Park JM, An JM, Paek KH (2002) Ectopic expression of Tsi1 in transgenic hot pepper plants enhances host resistance to viral, bacterial, and oomycete pathogens. MPMI 15(10):983–989
Sun AQ, Yi SY, Yang JY, Zhao CM, Liu J (2006) Identification and characterization of a heat-inducible ftsH gene from tomato (Lycopersicon esculentum Mill.). Plant Sci 170(3):551–562
Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M (2015) STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447-452
Tülek A, Özdemir FI, Ramadhan SS (2020) Cloning, expression and characterization of membrane bound FtsH protease of Geobacillus kaustophilus. Appl Biochem Microbiol 56(6):678–684
Ülker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7(5):491–498
Wang F, Liu J, Chen M, Zhou L, Li Z, Zhao Q, Pan G, Zaidi SH, Cheng F (2016) Involvement of abscisic acid in PSII photodamage and D1 protein turnover for light-induced premature senescence of rice flag leaves. PLoS ONE 11(8):e0161203
William Roy S, Gilbert W (2006) The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 7(3):211–221
Wu Q, Han T, Yang L, Wang Q, Zhao Y, Jiang D, Ruan X (2021) The essential roles of OsFtsH2 in developing the chloroplast of rice. BMC Plant Biol 21(1):1–4
Xiao JJ, Zhang RX, Khan A, Gai WX, Gong ZH (2021) CaFtsH06, a novel filamentous thermosensitive protease gene, is involved in heat, salt, and drought stress tolerance of pepper (Capsicum annuum L.). Int J Mol Sci 22(13):6953
Xing H, Jiang Y, Zou Y, Long X, Wu X, Ren Y, Li Y, Li HL (2021) Genome-wide investigation of the AP2/ERF gene family in ginger: evolution and expression profiling during development and abiotic stresses. BMC Plant Biol 21(1):1–21
Xue GP, Drenth J, McIntyre CL (2015) TaHsfA6f is a transcriptional activator that regulates a suite of heat stress protection genes in wheat (Triticum aestivum L.) including previously unknown Hsf targets. J Exp Bot 66(3):1025–1039
Yang Y, Guo R, Gaffney K, Kim M, Muhammednazaar S, Tian W, Wang B, Liang J, Hong H (2018) Folding-degradation relationship of a membrane protein mediated by the universally conserved ATP-dependent protease FtsH. J Am Chem Soc 140(13):4656–4665
Yang Z, Sun J, Chen Y, Zhu P, Zhang L, Wu S, Ma D, Cao Q, Li Z, Xu T (2019) Genome-wide identification, structural and gene expression analysis of the bZIP transcription factor family in sweet potato wild relative Ipomoea trifida. BMC Genet 20(1):1–8
Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, Yamane H, Shimono M, Sugano S, Takatsuji H, Kaku H (2013) WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64(16):5085–5097
Yoshioka-Nishimura M, Yamamoto Y (2014) Quality control of photosystem II: the molecular basis for the action of FtsH protease and the dynamics of the thylakoid membranes. J Photochem Photobiol B: Biol 137:100–106
Yu F, Park S, Rodermel SR (2004) The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. Plant J 37(6):864–876
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(2):855–63
Żelisko A, García-Lorenzo M, Jackowski G, Jansson S, Funk C (2005) AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. PNAS 102(38):13699–13704
Zhang J, Sun A (2009) Genome-wide comparative analysis of the metalloprotease ftsH gene families between Arabidopsis thaliana and rice. Shengwu Gongcheng Xuebao/chin J Biotechnol 25(9):1402–1408
Zhang S, Wu J, Yuan D, Zhang D, Huang Z, Xiao L, Yang C (2014) Perturbation of auxin homeostasis caused by mitochondrial FtSH4 gene-mediated peroxidase accumulation regulates Arabidopsis architecture. Mol Plant 7(5):856–873
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Hajibarat, Z., Saidi, A. Filamentation Temperature-Sensitive (FtsH); Key Player in Response to Multiple Environmental Stress Conditions and Developmental Stages in Potato. J Plant Growth Regul 42, 4223–4239 (2023). https://doi.org/10.1007/s00344-022-10885-x
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DOI: https://doi.org/10.1007/s00344-022-10885-x