Abstract
Tree peony (Paeonia suffruticosa) is an important and famous horticultural plant with ornamental, edible, and medicinal values. Drought is one of the main environmental stresses that affects various processes such as plant growth and productivity. The mechanism of drought tolerance has been studied in some plants and crops but not in tree peony. In this study, we identified an F-box protein in tree peony; the protein was named as PsFFL1 (PsF-box/FBD/LRR-repeat) based on the analysis of conserved domains, homologous sequence alignment and structure. Ectopic overexpression of PsFFL1 in tobacco plants demonstrated increased vigorous growth and drought tolerance, and it was significantly up-regulated under drought stress using quantitative RT-PCR (RT-qPCR) analysis. While, PsFFL1 was significantly down-regulated by exogenous naphthylacetic acid and gibberellin acid 3 treatment. Further, under normal or drought conditions, some drought stress-related genes including Late Embryogenesis Abundant5 (LEA5), no apical meristem (NAM), Arabidopsis transcription activation factor (ATAF), cup-shaped cotyledon 2 (CUC2) (NAC), Early Responsive to Dehydration 10 C (ERD10C), Calcium-Dependent Protein Kinase2 (CDPK2), WRKY28 and Osmotin were upregulated in the transgenic tobacco lines. Moreover, we preliminarily identified some drought-associated proteins such as Cu/Zn-superoxide dismutase (Cu/Zn-SOD), alcohol dehydrogenases 3 (ADH3), and heat shock proteins (HSPs), which could interact with PsFFL1 as revealed by pull down-mass spectrometry (MS). These results indicated that PsFFL1 plays a positive regulatory role in drought stress response in tree peony. The functions of most of the F-box proteins are not elucidated to date, and studies on F-box protein are currently focused on model plants or herbaceous plants. Therefore, this study is helpful to understand the molecular mechanism of involvement of F-box protein involved in drought tolerance and has the potential to be utilized in molecular breeding to improve drought stress tolerance in woody plants.
Key message
Overexpression of PsFFL1 enhanced drought tolerance in tobacco plants through upregulation of several stress-related genes and interaction with some drought-associated proteins.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated or analyzed during the current study are available from the corresponding author on reasonable request.
References
Alamri S, Hu Y, Mukherjee S, Aftab T, Fahad S, Raza A, Ahamd M, Siddiqui M. H (2020) Silicon-induced postponement of leaf senescence is accompanied by modulation of antioxidative defense and ion homeostasis in mustard (Brassica juncea) seedlings exposed to salinity and drought stress. Plant Physiol Biochem 157:47–59. https://doi.org/10.1016/j.plaphy.2020.09.038
Amoanimaa-Dede H, Shao Z, Su C, Yeboah A, Zhu H (2022) Genome-wide identification and characterization of F-box family proteins in sweet potato and its expression analysis under abiotic stress. Gene 817:146191. https://doi.org/10.1016/j.gene.2022.146191
An JP, Li R, Qu FJ, You CX, Wang XF, Hao YJ (2016) Apple F-Box protein MdMAX2 regulates plant photomorphogenesis and stress response. Front Plant Sci 7:1685. https://doi.org/10.3389/fpls.2016.01685
Bansal H, Bansal S, Rao M, Foley KP, Sang J, Proia D, Blackman RK, Ying W, Barsoum J, Baer MR, Kelly K, Swords R, Tomlinson GE, Battiwalla M, Giles FJ, Lee KP, Padmanabhan S (2010) Heat shock protein 90 regulates the expression of Wilms tumor 1 protein in myeloid leukemias. Blood 116(22):4591–4599. https://doi.org/10.1182/blood-2009-10-247239
Bashir MA, Silvestri C, Ahmad T, Hafiz IA, Abbasi NA, Manzoor A, Cristofori V, Rugini E (2020) Osmotin: a cationic protein leads to improve biotic and abiotic stress tolerance in plants. Plants (Basel) 9(8):992. https://doi.org/10.3390/plants9080992
Bernardo L, Carletti P, Badeck F.W, Rizza F, Morcia C, Ghizzoni R, Rouphael Y, Colla G, Terzi V, Lucini L (2019) Metabolomic responses triggered by arbuscular mycorrhiza enhance tolerance to water stress in wheat cultivars. Plant Physiol Biochem 137:203–212. https://doi.org/10.1016/j.plaphy.2019.02.007
Bubliy OA, Loesehche V (2005) Correlated responses to selection for stress resistance and longevity in a laboratory population of Drosophila melanogaste. J Exp Bot 18(4):789–803. https://doi.org/10.1111/j.1420-9101.2005.00928.x
Chen P, Tu X, Akdemir F, Chew SK, Rothenfluh A, Abrams JM (2012) Effectors of alcohol-induced cell killing in Drosophila. Cell Death Differ 19(10):1655–1663. https://doi.org/10.1038/cdd.2012.47
Chen C, Wu C, Miao J, Lei Y, Zhao D, Sun D, Yang G, Huang J, Zheng C (2014) Arabidopsis SAG protein containing the MDN1 domain participates in seed germination and seedling development by negatively regulating ABI3 and ABI5. J Exp Bot 65(1):35–45. https://doi.org/10.1093/jxb/ert343
Chen YS, Lo SF, Sun PK, Lu CA, Ho TH, Yu SM (2015) A late embryogenesis abundant protein HVA1 regulated by an inducible promoter enhances root growth and abiotic stress tolerance in rice without yield penalty. Plant Biotechnol J 13(1):105–116. https://doi.org/10.1111/pbi.12241
Chen Z, Liu Y, Yin Y, Liu Q, Li N, Li X, He W, Hao D, Liu X, Guo C (2019) Expression of AtGA2ox1 enhances drought tolerance in maize. Plant Growth Regul 89:203–215. https://doi.org/10.1007/s10725-019-00526-x
Chen J, Li Y, Li Y, Li Y, Wang Y, Jiang C, Choisy P, Xu T, Cai Y, Pei D, Jiang CZ, Gan SS, Gao J, Ma N (2021a) AUXIN RESPONSE FACTOR 18-HISTONE DEACETYLASE 6 module regulates floral organ identity in rose (Rosa hybrida). Plant Physiol 186(2):1074–1087. https://doi.org/10.1093/plphys/kiab130
Chen X, Wang Z, Tang R, Wang L, Chen C, Ren Z (2021b) Genome-wide identification and expression analysis of Hsf and Hsp gene families in cucumber (Cucumis sativus L.). Plant Growth Regul 95:223–239. https://doi.org/10.1007/s10725-021-00739-z
Chevilly S, Dolz-Edo L, Martínez-Sánchez G, Morcillo L, Vilagrosa A, López-Nicolás JM, Blanca J, Yenush L, Mulet JM (2021) Distinctive traits for Drought and Salt stress tolerance in Melon (Cucumis melo L.). Front Plant Sci 12:777060. https://doi.org/10.3389/fpls.2021.777060
Chunthong K, Pitnjam K, Chakhonkaen S (2017) Differential drought responses in F-box gene expression and grain yield between two rice groups with contrasting drought tolerance. J Plant Growth Regul 36:970–982. https://doi.org/10.1007/s00344-017-9701-y
Cieśla A, Mituła F, Misztal L, Fedorowicz-Strońska O, Janicka S, Tajdel-Zielińska M, Marczak M, Janicki M, Ludwików A, Sadowski J (2016) A role for barley calcium-dependent protein kinase CPK2a in the response to drought. Front Plant Sci 7:1550. https://doi.org/10.3389/fpls.2016.01550
Du SB (2016) The physiological and bBiochemical effects on Paeonia ostii under waterlogging stress and restoration. Dissertation, Master’s Thesis East China Normal University, Shanghai, China
Fan G, Xia X, Yao W, Cheng Z, Zhang X, Jiang J, Zhou B, Jiang T (2022) Genome-wide identification and expression patterns of the F-box family in Poplar under salt stress. Int J Mol Sci 23(18):10934. https://doi.org/10.3390/ijms231810934
Gagne JM, Downes BP, Shiu SH, Durski AM, Vierstra RD (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. PNAS 99(17):11519–11524. https://doi.org/10.1073/pnas.162339999
Gao S, Song JB, Wang Y, Yang ZM (2017) An F-box E3 ubiquitin ligase-coding gene AtDIF1 is involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner. Environ Exp Bot 138:21–35. https://doi.org/10.1016/j.envexpbot.2017.02.013
Gu Z, Men S, Zhu J, Hao Q, Tong N, Liu ZA, Zhang H, Shu Q, Wang L (2019) Chalcone synthase is ubiquitinated and degraded via interactions with a RING-H2 protein in petals of Paeonia ‘he Xie’. J Exp Bot 70(18):4749–4762. https://doi.org/10.1093/jxb/erz245
Guan Y, Leu NA, Ma J, Chmátal L, Ruthel G, Bloom JC, Lampson MA, Schimenti JC, Luo M, Wang PJ (2020) SKP1 drives the prophase I to metaphase I transition during male meiosis. Sci Adv 6(13):eaaz2129. https://doi.org/10.1126/sciadv.aaz2129
Guo L, Guo D, Yin W, Hou X (2018) Tolerance strategies revealed in tree peony (Paeonia suffruticosa; Paeoniaceae) ecotypes differentially adapted to desiccation. Appl Plant Sci 6(10):e01191. https://doi.org/10.1002/aps3.1191
Gupta S, Garg V, Kant C, Bhatia S (2015) Genome-wide survey and expression analysis of F-box genes in chickpea. BMC genomics 16(1):67. https://doi.org/10.1186/s12864-015-1293-y
Han XY, Wang LS, Shu QY, Liu ZA, Xu SX, Tetsumura T (2008) Molecular characterization of tree peony germplasm using sequence-related amplified polymorphism markers. Biochem Genet 46(3-4):162-79. https://doi.org/10.1007/s10528-007-9140-8
Hennig L (2012) Plant gene regulation in response to abiotic stress. Biochim Biophys Acta 1819(2): 85. https://doi.org/10.1016/j.bbagrm.2012.01.005
Hirofumi K, Naoki T, Hiroaki S, Motoaki S, Kazuo S, M (2002) Classification and expression analysis of Arabidopsis F-Box-Containing protein genes. Plant Cell Physiol 10:1073–1085. https://doi.org/10.1093/pcp/pcf151
Horsch R.B, Wallroth M (1985) A simple and general method for transferring genes into plants. Science 227(4691):1229–31. https://doi.org/10.1126/science.227.4691.1229
Hu XL, Li YH, Yang HR, Liu QJ, Li CH (2010) Heat shock protein 70 may improve the ability of antioxidant defense in duced by the combination of drought and heat in maize leaves. College of Life Science 36 (4):636–644 (In Chinese with English abstract). https://doi.org/10.3724/SP.J.1006.2010.00636
Jia F, Wu B, Li H, Huang J, Zheng C (2013) Genome-wide identification and characterization of F-box family in maize. Mol Genet 288:559–577. https://doi.org/10.1007/s00438-013-0769-1
Jia Q, Xiao ZX, Wong FL, Sun S, Liang KJ, Lam HM (2017) Genome-wide analyses of the soybean F-Box gene family in response to salt stress. Int J Mol Sci 18(4):818. https://doi.org/10.3390/ijms18040818
Jiang Z, Liu D, Wang T, Liang X, Cui Y, Liu Z, Li W (2020) Concentration difference of auxin involved in stem development in soybean. J Integr Agr 19:953–964. https://doi.org/10.1016/S2095-3119(19)62676-6
Kato-Noguchi H, Yasuda Y (2007) Effect of low temperature on ethanolic fermentation in rice seedlings. J Plant Physiol 164:1013–1018. https://doi.org/10.1016/j.jplph.2006.06.007
Kim YY, Cui MH, Noh MS, Jung KW, Shin JS (2017) The FBA motif-containing protein AFBA1 acts as a novel positive regulator of ABA response in Arabidopsis. Plant Cell Physiol 58(3):574–586. https://doi.org/10.1093/pcp/pcx003
Kim H, Yu SI, Jung SH, Lee BH, Suh MC (2019) The F-Box protein SAGL1 and ECERIFERUM3 regulate cuticular wax biosynthesis in response to changes in humidity in Arabidopsis. Plant Cell 31(9):2223–2240. https://doi.org/10.1105/tpc.19.00152
Komatsu S, Thibaut D, Hiraga S, Kato M, Chiba M, Hashi-guchi A, Tougou M, Shimamura S, Yasue H (2011) Characterization of a novel flooding stress-responsive alcohol dehydrogenase expressed in soybean roots. Plant Mol Biol 77:309–322. https://doi.org/10.1007/s11103-011-9812-y
Kong X, Zhou S, Yin S, Zhao Z, Han Y, Wang W (2016) Stress-inducible expression of an F-box gene TaFBA1 from wheat enhanced the drought tolerance in transgenic tobacco plants without impacting growth and development. Front Plant Sci 7:1295. https://doi.org/10.3389/fpls.2016.01295
Koops P, Pelser S, Ignatz M, Klose C, Marrocco-Selden K, Kretsch T (2011) EDL3 is an F-box protein involved in the regulation of abscisic acid signalling in Arabidopsis thaliana. J Exp Bot 62(15):5547–60. https://doi.org/10.1093/jxb/err236
Kürsteiner O, Dupuis I, Kuhlemeier C (2003) The pyruvate decarboxylase1 gene of Arabidopsis is required during anoxia but not other environmental stresses. Plant Physiol 132:968–978. https://doi.org/10.1104/pp.102.016907
Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Li-causi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata F (2007) Transcript profiling of the anoxic rice coleoptiles. Plant Physiol 144:218–231. https://doi.org/10.1104/pp.106.093997
Laskowski M, Biller SJ, Stanley K, Kajstura TJ, Prusty R (2006). Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol 476:788–92. https://doi.org/10.1093/PCP/PCJ043
Li J, Zhang X, Zhao X (2011) Tree peony in China, 20–22. Encyclopedia of China Publishing House, Beijing, China
Li W, Li X, Chao J, Zhang Z, Wang W, Guo Y (2018) NAC family transcription factors in tobacco and their potential role in regulating leaf senescence. Front Plant Sci 9:1900. https://doi.org/10.3389/fpls.2018.01900
Li W, Chen Y, Ye M, Wang D, Chen Q (2020a) Evolutionary history of the heat shock protein 90 (Hsp90) family of 43 plants and characterization of Hsp90s in Solanum tuberosum. Mol Biol Rep 47(9):6679–6691. https://doi.org/10.1007/s11033-020-05722-x
Li Y, Liu F, Li P, Wang T, Zheng C, Hou B (2020b) An Arabidopsis cytokinin-modifying glycosyltransferase UGT76C2 improves drought and salt tolerance in rice. Front Plant Sci 11:560696. https://doi.org/10.3389/fpls.2020b.560696
Li M, Yang Y, Raza A, Yin S, Wang H, Zhang Y, Zhang H (2021a) Heterologous expression of Arabidopsis thaliana rty gene in strawberry (Fragaria×ananassa Duch.) Improves drought tolerance. BMC Plant Biology 21:57. https://doi.org/10.1186/s12870-021-02839-4
Li ZQ, Zhang Y, Li H, Su TT, Liu CG, Han ZC, Wang AY, Zhu JB (2021b) Genome-wide characterization and expression analysis provide basis to the biological function of cotton FBA genes. Front Plant Sci 12:696698. https://doi.org/10.3389/fpls.2021b.696698
Li BW, Gao S, Yang ZM, Song JB (2022). The F-box E3 ubiquitin ligase AtSDR is involved in salt and drought stress responses in Arabidopsis. Gene 809:146011. https://doi.org/10.1016/j.gene.2021.146011
Liu H, Ma G, Zhu K, Zou QC, Zhou JH, Tian DQ (2016) Functional analysis of stress-related transcription factor gene PsDREB from Paeonia suffruticosa. Journal of Zhejiang University (Agric. & Life Sci., in Chinese with English abstract) 42(6):679–686. https://doi.org/10.3785/j.issn.1008-9209.2015.05.152.
Liu G, Li B, Li X, Wei Y, He C, Shi H (2020) MaWRKY80 positively regulates plant drought stress resistance through modulation of abscisic acid and redox metabolism. Plant Physiol Biochem 156:155–166. https://doi.org/10.1016/j.plaphy.2020.09.015
Magen D, Georgopoulos C, Bross P, Ang D, Segev Y, Goldsher D, Nemirovski A, Shahar E, Ravid S, Luder A, Heno B, Gershoni-Baruch R, Skorecki K, Mandel H (2008) Mitochondrial hsp60 chaperonopathy causes an autosomal-recessive neurodegenerative disorder linked to brain hypomyelination and leukodystrophy. Am J Hum Genet 83(1):30–42. https://doi.org/10.1016/j.ajhg.2008.05.016
Maheswari M, Varalaxmi Y, Vijayalakshmi A, Yadav S. K, Sharmila P, Venkateswarlu B, Vanaja M, Pardha Saradhi P (2010) Metabolic engineering using mtlD gene enhances tolerance to water deficit and salinity in sorghum. Biol Plant 54:647–652. https://doi.org/10.1007/s10535-010-0115-y
Mei C, Jiang SC, Lu YF, Wu FQ, Yu YT, Liang S, Feng XJ, Portoles Comeras S, Lu K, Wu Z, Wang XF, Zhang DP (2014) Arabidopsis pentatricopeptide repeat protein SOAR1 plays a critical role in abscisic acid signaling. J Exp Bot 65(18):5317–5330. https://doi.org/10.1093/jxb/eru293
Parkhi V, Kumar V, Sunilkumar G, Campbell LM, Singh NK (2009) Expression of apoplastically secreted tobacco osmotin in cotton confers drought tolerance. Mol Breeding 23:625–639. https://doi.org/10.1007/s11032-009-9261-3
Priji PJ, Hemaprabha G (2015) Sugarcane specific drought responsive candidate genes belonging to ABA dependent pathway identified from basic species clones of Saccharum sp. and Erianthus sp. Sugar Tech 17:130–137. https://doi.org/10.1007/s12355-014-0313-6
Qu L, Sun M, Li X, He R, Zhong M, Luo D, Liu X, Zhao X (2020). The Arabidopsis F-box protein FOF2 regulates ABA-mediated seed germination and drought tolerance. Plant Sci 301:110643. https://doi.org/10.1016/j.plantsci.2020.110643
Quan W, Liu X, Wang H, Chan Z (2015) Comparative physiological and transcriptional analyses of two contrasting drought tolerant alfalfa warieties. Front Plant Sci 6:1256. https://doi.org/10.3389/fpls.2015.01256
Raza A, Mubarik MS, Sharif R, Habib M, Jabeen W, Zhang C, Chen H, Chen ZH, Siddique KHM, Zhuang W, Varshney RK (2022) Developing drought-smart, ready-to-grow future crops. Plant Genome 10:e20279. https://doi.org/10.1002/tpg2.20279
Rogers A (1995) Peonies. Timber Press, Portland, Oregon, USA
Rombolá-Caldentey B, Rueda-Romero P, Iglesias-Fernández R, Carbonero P, Oñate-Sánchez L (2014) Arabidopsis DELLA and two HD-ZIP transcription factors regulate GA signaling in the epidermis through the L1 box cis-element. Plant Cell 26(7):2905–2919. https://doi.org/10.1105/tpc.114.127647
Sanadhya P, Kumar A, Bucki P, Fitoussi N, Carmeli-Weissberg M, Borenstein M, Brown-Miyara S (2021) Tomato divinyl ether-biosynthesis pathway is implicated in modulating of root-knot nematode meloidogyne javanica’s parasitic ability. Front Plant Sci 12:670772. https://doi.org/10.3389/fpls.2021.670772
Schumann N, Navarro-Quezada A, Ullrich K, Kuhl C, Quint M (2011) Molecular evolution and selection patterns of plant F-box proteins with C-terminal kelch repeats. Plant physiol 155(2):835–850. https://doi.org/10.1104/pp.110.166579
Shan YJ, Li D, Cao JJ, Cao J, Zhang L, Han LQ, Han L, Zhang MP, Zhang M, Shen ZG (2022) Over-expression of Arabidopsis ORANGE gene enhances drought stress tolerance through ABA-dependent pathway in Arabidopsis thaliana. Plant Growth Regul 96:91–101. https://doi.org/10.1007/s10725-021-00760-2
Shen X, Guo X, Zhao D, Zhang Q, Jiang Y, Wang Y, Peng X, Wei Y, Zhai Z, Zhao W, Li, T (2017) Cloning and expression profiling of the PacSnRK2 and PacPP2C gene families during fruit development, ABA treatment, and dehydration stress in sweet cherry. Plant Physiol Biochem 119:275–285. https://doi.org/10.1016/j.plaphy.2017.08.025
Shu QY, Wischnitzki E, Liu ZA, Ren HX, Han XY, Hao Q, Gao FF, Xu SX, Wang LS (2009) Functional annotation of expressed sequence tags as a tool to understand the molecular mechanism controlling flower bud development in tree peony. Physiol Plant 135(4):436–49. https://doi.org/10.1111/j.1399-3054.2009.01206.x
Song Y, Liu L, Wei Y, Li G, Yue X, An L (2017) Metabolite Profiling of adh1 Mutant Response to Cold Stress in Arabidopsis. Front Plant Sci 7:2072. https://doi.org/10.3389/fpls.2016.02072
Stefanowicz K, Lannoo N, Proost P, Van Damme EJM (2012). Arabidopsis F-box protein containing a Nictaba-related lectin domain interacts with N-acetyllactosamine structures. FEBS Open Bio 2:151–158. https://doi.org/10.1016/j.fob.2012.06.002
Su J, Ma C, Liu C, Gao C, Nie R, Wang H (2016) Hypolipidemic activity of peony seed oil rich in α-Linolenic, is mediated through inhibition of lipogenesis and upregulation of fatty acid β-Oxidation. J Food Sci 81(4):H1001–H1009. https://doi.org/10.1111/1750-3841.13252
Trujillo JT, Beilstein MA, Mosher RA (2016) The Argonaute-binding platform of NRPE1 evolves through modulation of intrinsically disordered repeats. New Phytol 212(4):1094–1105. https://doi.org/10.1111/nph.14089
Wang LQ (2014) A functional analysis of F-box gene At5g22700 in Arabidopsis. Dissertation, HuNan University, Changsha, China
Wang X, Liu XF, Zhou YJ, Zhang GF (2014) Molecular mechanism of expression and regulation of SOD gene in plant. Chinese J Oil Crop Sci 36(2):275–280. https://doi.org/10.7505/j.issn.1007-9084.2014.02.021
Wang GM, Yin H, Qiao X, Tan X, Gu C, Wang BH, Cheng R, Wang YZ, Zhang SL (2016) F-box genes: genome-wide expansion, evolution and their contribution to pollen growth in pear (Pyrus bretschneideri). Plant Sci 253:164–175. https://doi.org/10.1016/j.plantsci.2016.09.009
Wang F, Wang JW, Sun LJ, Song XS (2019) The molecular cloning and functional characterization of ChNAC1, a NAC transcription factor in Cerasus humilis. Plant Growth Regul 89:331–343. https://doi.org/10.1007/s10725-019-00536-9
Wild M, Davière JM, Cheminant S, Regnault T, Baumberger N, Heintz D, Baltz R, Genschik P, Achard P (2012) The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 24(8):3307–19. https://doi.org/10.1105/tpc.112.101428
Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EM, Maier A, Schwechheimer C (2007) The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19(4):1209–20. https://doi.org/10.1105/tpc.107.051441
Xiao H, Wang H, Silva EA, Thompson J, Guillou A, Yates JR Jr, Buchon N, Franc NC (2015) The Pallbearer E3 ligase promotes actin remodeling via RAC in efferocytosis by degrading the ribosomal protein S6. Dev Cell 32(1):19–30. https://doi.org/10.1016/j.devcel.2014.11.015
Xu G, Ma H, Nei M, Kong H (2009) Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. PNAS 106(3):835–840. https://doi.org/10.1073/pnas.0812043106
Xu Z, Raza Q, Xu L, He X, Huang Y, Yi J, Zhang D, Shao HB, Ma H, Ali Z (2018) GmWRKY49, a salt-responsive nuclear protein, improved root length and governed better salinity tolerance in transgenic Arabidopsis. Front Plant Sci 9:809. https://doi.org/10.3389/fpls.2018.00809
Yu Y, Wang P, Bai Y, Wang Y, Wan H, Liu C, Ni Z (2020) The soybean F-box protein GmFBX176 regulates ABA-mediated responses to drought and salt stress. Environ Exp Bot 176:104056. https://doi.org/10.1016/j.envexpbot.2020.104056
Zeng XU, Liu ZG, Shi PH, Xu YZ (2014) Cloning and expression analysis of copper and zinc superoxide dismutase (Cu/Zn-SOD) gene from Brassica campestris L. Acta Agronomica Sinica 40(4):636–643. https://doi.org/10.3724/SP.J.1006.2014.00636
Zhang L, Xiao S, Li W, Feng W, Li J, Wu Z, Gao X, Liu F, Shao, M (2011) Overexpression of a Harpin-encoding gene hrf1 in rice enhances drought tolerance. J Exp Bot 62(12):4229–4238. https://doi.org/10.1093/jxb/err131
Zhang Y, Lan H, Shao Q, Wang R, Chen H, Tang H, Zhang HS, Huang J (2016) An A20/AN1-type zinc finger protein modulates gibberellins and abscisic acid contents and increases sensitivity to abiotic stress in rice (Oryza sativa). J Exp Bot 67:315–326. https://doi.org/10.1093/jxb/erv464
Zhang C, Yang R, Zhang T, Zheng D, Li X, Zhang Z, Li l, Wu Z (2023) ZmTIFY16, a novel maize TIFY transcription factor gene, promotes root growth and development and enhances drought and salt tolerance in Arabidopsis and Zea mays. Plant Growth Regul 100:49-160. https://doi.org/10.1007/s10725-022-00946-2
Zhao D, Luan Y, Shi W, Zhang X, Meng J, Tao J (2021) A Paeonia ostii caffeoyl-CoA O-methyltransferase confers drought stress tolerance by promoting lignin synthesis and ROS scavenging. Plant Sci 303:110765. https://doi.org/10.1016/j.plantsci.2020.110765
Zheng F, Cui X, Rivarola M, Gao T, Chang C, Dong CH (2017) Molecular association of Arabidopsis RTH with its homolog RTE1 in regulating ethylene signaling. J Exp Bot 68(11):2821–2832. https://doi.org/10.1093/jxb/erx175
Zhou Y, Karl T, Lewis DH, McGhie TK, Arathoon S, Davies KM, Ryan KG, Gould KS, Schwinn KE (2021) Production of betacyanins in transgenic Nicotiana tabacum increases tolerance to salinity. Front Plant Sci 12:653147. https://doi.org/10.3389/fpls.2021.653147
Zhu F, Li M, Yan M, Qiao F, Jiang X (2021) Integrated transcriptome analysis and single-base resolution methylomes of watermelon (Citrullus lanatus) reveal epigenome modifications in response to osmotic stress. Front Plant Sci 12:769712. https://doi.org/10.3389/fpls.2021.769712
Funding
This work was supported by the National Natural Science Foundation of China (32072065 and 30800760).
Author information
Authors and Affiliations
Contributions
YL, QH and QS conceived and designed research. XZ, YL and XW conducted the experiments. ZL prepared and cultivated the materials. QH and PL analyzed data. XZ, YL wrote the manuscript and QS, QH revised the manuscript. All the authors read and approve the manuscript.
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
All experimental studies on plants have complied with relevant institutional, national, and international guidelines and legislation. All authors have read and agreed to the published version of the manuscript.
Competing interests
There is no competing interest in the publication of this manuscript.
Additional information
Communicated by Baris Uzilday.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
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
Zhang, X., Li, Y., Wang, X. et al. Overexpression of a novel F-box protein PsFFL1 from tree peony (Paeonia suffruticosa) confers drought tolerance in tobacco. Plant Growth Regul 101, 131–143 (2023). https://doi.org/10.1007/s10725-023-01007-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-023-01007-y