A secreted catalase contributes to Puccinia striiformis resistance to host-derived oxidative stress

Pu Yuan, Wenhao Qian, Lihua Jiang, Conghui Jia, Xiaoxuan Ma, Zhensheng Kang, Jie Liu

Stress Biology ›› 2021, Vol. 1 ›› Issue (1) : 22. DOI: 10.1007/s44154-021-00021-2
Original Paper

A secreted catalase contributes to Puccinia striiformis resistance to host-derived oxidative stress

Author information +
History +

Abstract

Plants can produce reactive oxygen species (ROS) to counteract pathogen invasion, and pathogens have also evolved corresponding ROS scavenging strategies to promote infection and pathogenicity. Catalases (CATs) have been found to play pivotal roles in detoxifying H2O2 formed by superoxide anion catalyzed by superoxide dismutases (SODs). However, few studies have addressed H2O2 removing during rust fungi infection of wheat. In this study, we cloned a CAT gene PsCAT1 from Puccinia striiformis f. sp. tritici (Pst), which encodes a monofunctional heme-containing catalase. PsCAT1 exhibited a high degree of tolerance to pH and temperature, and forms high homopolymers.

Heterologous complementation assays in Saccharomyces cerevisiae reveal that the signal peptide of PsCAT1 is functional. Overexpression of PsCAT1 enhanced S. cerevisiae resistance to H2O2. Transient expression of PsCAT1 in Nicotiana benthamiana suppressed Bax-induced cell death. Knockdown of PsCAT1 using a host-induced gene silencing (HIGS) system led to the reduced virulence of Pst, which was correlated to H2O2 accumulation in HIGS plants. These results indicate that PsCAT1 acts as an important pathogenicity factor that facilitates Pst infection by scavenging host-derived H2O2.

Keywords

Wheat stripe rust / Puccinia striiformis f. sp. tritici / Catalase / Reactive oxygen species / Host-induced gene silencing

Cite this article

Download citation ▾
Pu Yuan, Wenhao Qian, Lihua Jiang, Conghui Jia, Xiaoxuan Ma, Zhensheng Kang, Jie Liu. A secreted catalase contributes to Puccinia striiformis resistance to host-derived oxidative stress. Stress Biology, 2021, 1(1): 22 https://doi.org/10.1007/s44154-021-00021-2

References

[1]
BenoitSL, MaierRJ. Helicobacter catalase devoid of catalytic activity protects the bacterium against oxidative stress. J Biol Chem, 2016, 291(45):23366-23373
CrossRef Google scholar
[2]
CaleraJA, ParisS, MonodM, HamiltonAJ, DebeaupuisJP, DiaquinM, López-MedranoR, LealF, LatgéJP. Cloning and disruption of the antigenic catalase gene of Aspergillus fumigatus. Infect Immun, 1997, 65(11):4718-4724
CrossRef Google scholar
[3]
ChangQ, LiuJ, LinXH, HuSJ, YangY, LiD, ChenLY, HuaiBY, HuangLL, VoegeleRT, KangZS. A unique invertase is important for sugar absorption of an obligate biotrophic pathogen during infection. New Phytol, 2017, 215(4):1548-1561
CrossRef Google scholar
[4]
ChelikaniP, FitaI, LoewenPC. Diversity of structures and properties among catalases. Cell Mol Life Sci, 2004, 61(2):192-208
CrossRef Google scholar
[5]
Cuéllar-CruzM, Briones-Martin-del-CampoM, Cañas-VillamarI, Montalvo-ArredondoJ, Riego-RuizL, CastañoI, De LasPA. High resistance to oxidative stress in the fungal pathogen Candida glabrata is mediated by a single catalase, Cta1p, and is controlled by the transcription factors Yap1p, Skn7p, Msn2p, and Msn4p. Eukaryot Cell, 2008, 7(5):814-825
CrossRef Google scholar
[6]
Dong W, Hou Y, Li S, Wang F, Zhou J, Li Z, Wang Y, Huang F, Fu L, Huang Y, Cui Z (2015) Purification, cloning, expression, and biochemical characterization of a monofunctional catalase, KatP, from Pigmentiphaga sp. DL-8. Protein Expr Purif 108:54–61. https://doi.org/10.1016/j.pep.2015.01.011
[7]
FoyerCH, NoctorG. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell, 2005, 17(7):1866-1875
CrossRef Google scholar
[8]
GarreV, MüllerU, TudzynskiP. Cloning, characterization and targeted disruption of cpcat1, coding for an in planta secreted catalase of Claviceps purpurea. Mol Plant-Microbe Interact, 1998, 11(8):772-783
CrossRef Google scholar
[9]
GonzálezJ, CastilloR, García-CamposMA, Noriega-SamaniegoD, Escobar-SánchezV, Romero-AguilarL, Alba-LoisL, Segal-KischinevzkyC. Tolerance to oxidative stress in budding yeast by heterologous expression of catalases a and T from Debaryomyces hansenii. Curr Microbiol, 2020, 77(12):4000-4015
CrossRef Google scholar
[10]
GuB, KaleSD, WangQH, WangDH, PanQN, CaoH, CaoH, MengYL, KangZS, TylerBM, ShanWX. Rust secreted protein Ps87 is conserved in diverse fungal pathogens and contains a RXLR like motif sufficient for translocation into plant cells. PLoS One, 2011, 6(11):e27217
CrossRef Google scholar
[11]
GuoY, YaoS, YuanT, WangYZ, ZhangD, TangWH. The spatiotemporal control of KatG2 catalase-peroxidase contributes to the invasiveness of fusarium graminearum in host plants. Mol Plant Pathol, 2019, 20(5):685-700
CrossRef Google scholar
[12]
HolzbergS, BrosioP, GrossC, PogueGP. Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J, 2002, 30(3):315-327
CrossRef Google scholar
[13]
JamiesonDJ. Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast, 1998, 14(16):1511-1527
CrossRef Google scholar
[14]
KapetanakiSM, ZhaoX, YuS, MagliozzoRS, SchelvisJP. Modification of the active site of mycobacterium tuberculosis KatG after disruption of the met-Tyr-Trp cross-linked adduct. J Inorg Biochem, 2007, 101(3):422-433
CrossRef Google scholar
[15]
KawasakiL, WysongD, DiamondR, AguirreJ. Two divergent catalase genes are differentially regulated during aspergillus nidulans development and oxidative stress. J Bacteriol, 1997, 179(10):3284-3292
CrossRef Google scholar
[16]
LeeDH, OhDC, OhYS, MalinverniJC, KukorJJ, KahngHY. Cloning and characterization of monofunctional catalase from photosynthetic bacterium Rhodospirillum rubrum S1. J Microbiol Biotechnol, 2007, 17(9):1460-14688
[17]
LiuJ, GuanT, ZhengPJ, ChenLY, YangY, HuaiBY, LiD, ChangQ, HuangLL, KangZS. An extracellular Zn-only superoxide dismutase from Puccinia striiformis confers enhanced resistance to host-derived oxidative stress. Environ Microbiol, 2016, 18(11):4118-4135
CrossRef Google scholar
[18]
MittlerR. ROS are good. Trends Plant Sci, 2017, 22(1):11-19
CrossRef Google scholar
[19]
MittlerR, VanderauweraS, GolleryM, VanBF. Reactive oxygen gene network of plants. Trends Plant Sci, 2004, 9(10):490-498
CrossRef Google scholar
[20]
MontibusM, Pinson-GadaisL, Richard-ForgetF, BarreauC, PontsN. Coupling of transcriptional response to oxidative stress and secondary metabolism regulation in filamentous fungi. Crit Rev Microbiol, 2015, 41(3):295-308
CrossRef Google scholar
[21]
Morales HernandezCE, Padilla GuerreroIE, Gonzalez HernandezGA, Salazar SolisE, Torres GuzmanJC. Catalase overexpression reduces the germination time and increases the pathogenicity of the fungus Metarhizium ansiopliae. Appl Microbiol Biotechnol, 2010, 87(3):1033-1044
CrossRef Google scholar
[22]
NathuesE, JoshiS, TenbergeKB, von den DrieschM, OeserB, BäumerN, MihlanM, TudzynskiP. CPTF1, a CREB-like transcription factor, is involved in the oxidative stress response in the phytopathogen Claviceps purpurea and modulates ROS level in its host Secale cereale. Mol Plant-Microbe Interact, 2004, 17(4):383-393
CrossRef Google scholar
[23]
Navarro RE, Stringer MA, Hansberg W, Timberlake WE, Aguirre J (1996) CatA, a new Aspergillus nidulans gene encoding a developmentally regulated catalase. Curr Genet 29(4):352–359
[24]
NichollsP, FitaI, LoewenPC. Enzymology and structure of catalases. Adv Inorg Chem, 2001, 51: 51-106
CrossRef Google scholar
[25]
OhSK, YoungC, LeeM, OlivaR Bozkurt TO CanoLM, WinJ, BosJI, LiuHY, van DammeM, MorganW, ChoiD, Van der VossenEA, VleeshouwersVG, KamounS. In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell, 2009, 21(9):2928-2947
CrossRef Google scholar
[26]
SchererM, WeiH, LieseR, FischerR. Aspergillus nidulans catalase-peroxidase gene (cpeA) is transcriptionally induced during sexual development through the transcription factor StuA. Eukaryot Cell, 2002, 1(5):725-735
CrossRef Google scholar
[27]
SkamniotiP, HendersonC, ZhangZ, RobinsonZ, GurrSJ. A novel role for catalase B in the maintenance of fungal cell-wall integrity during host invasion in the rice blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact, 2007, 20(5):568-580
CrossRef Google scholar
[28]
SoochBS, KauldharBS, PuriM. Recent insights into microbial catalases: isolation, production and purification. Biotechnol Adv, 2014, 32(8):1429-1447
CrossRef Google scholar
[29]
TanabeS, Ishii-MinamiN, SaitohK, OtakeY, KakuH, ShibuyaN, NishizawaY, MinamiE. The role of catalase-peroxidase secreted by Magnaporthe oryzae during early infection of rice cells. Mol Plant-Microbe Interact, 2011, 24(2):163-171
CrossRef Google scholar
[30]
VetranoAM, HeckDE, MarianoTM, MishinV, LaskinDL, LaskinJD. Characterization of the oxidase activity in mammalian catalase. J Biol Chem, 2005, 280(42):35372-35381
CrossRef Google scholar
[31]
WaadtR, SchmidtLK, LohseM, HashimotoK, BockR, KudlaJ. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J, 2008, 56(3):505-516
CrossRef Google scholar
[32]
WangCF, HuangLL, BuchenauerH, HanQM, ZhangHC, KangZS. Histochemical studies on the accumulation of reactive oxygen species (O2 and H2O2) in the incompatible and compatible interaction of wheat-Puccinia striiformis f. sp. tritici. Physiol Mol Plant Pathol, 2007, 71(4-6):230-239
CrossRef Google scholar
[33]
WangGF, FanR, WangX, WangD, ZhangX. TaRAR1 and TaSGT1 associate with TaHsp90 to function in bread wheat (Triticum aestivum L.) seedling growth and stripe rust resistance. Plant Mol Biol, 2015, 87(6):577-589
CrossRef Google scholar
[34]
WangZL, ZhangLB, YingSH, FengMG. Catalases play differentiated roles in the adaptation of a fungal entomopathogen to environmental stresses. Environ Microbiol, 2013, 15(2):409-418
CrossRef Google scholar
[35]
WysongDR, ChristinL, SugarAM, RobbinsPW, DiamondRD. Cloning and sequencing of a Candida albicans catalase gene and effects of disruption of this gene. Infect Immun, 1998, 66(5):1953-1961
CrossRef Google scholar
[36]
YamashitaK, ShiozawaA, BannoS, FukumoriF, IchiishiA, KimuraM, FujimuraM. Involvement of OS-2 MAP kinase in regulation of the large-subunit catalases CAT-1 and CAT-3 in Neurospora crassa. Genes Genet Syst, 2007, 82(4):301-310
CrossRef Google scholar
[37]
YangH, ZhangX, MaZ, XuN, LiuJ. Expression, purification and characterization of catalase from Corynebacterium glutamicum. Chin J Biotechnol, 2020, 36(8):1568-1577
CrossRef Google scholar
[38]
YuC, WangN, WuM, TianF, ChenH, YangF, YuanX, YangCH, HeC. OxyR-regulated catalase CatB promotes the virulence in rice via detoxifying hydrogen peroxide in Xanthomonas oryzae pv. Oryzae. BMC Microbiol, 2016, 16(1):269
CrossRef Google scholar
[39]
YuanF, YinS, XuY, XiangL, WangH, LiZ, LiZ, FanK, PanG. The richness and diversity of catalases in Bacteria. Front Microbiol, 2021, 12: 645477
CrossRef Google scholar
[40]
ZámockýM, KollerF. Understanding the structure and function of catalases: clues from molecular evolution and in vitro mutagenesis. Prog Biophys Mol Biol, 1999, 72(1):19-66
CrossRef Google scholar
[41]
ZhangZ, HendersonC, GurrSJ. Blumeria graminis secretes an extracellular catalase during infection of barley: potential role in suppression of host defence. Mol Plant Pathol, 2004, 5(6):537-547
CrossRef Google scholar
[42]
ZhengP, ChenL, ZhongSX, WeiXB, ZhaoQ, PanQL, KangZS, LiuJ. A cu-only superoxide dismutase from stripe rust fungi functions as a virulence factor deployed for counter defense against host-derived oxidative stress. Environ Microbiol, 2020, 22(12):5309-5326
CrossRef Google scholar
[43]
ZhengWM, HuangLL, HuangJQ, WangXJ, ChenXM, ZhaoJ, GuoJ, ZhuangH, QiuC, LiuJ, LiuH, HuangX, PeiG, ZhanG, TangC, ChengY, LiuM, ZhangJ, ZhaoZ, ZhangS, HanQ, HanD, ZhangH, ZhaoJ, GaoX, WangJ, NiP, DongW, YangL, YangH, XuJR, ZhangG, KangZ. High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus. Nat Commun, 2013, 4(1):2673
CrossRef Google scholar
[44]
ZhuZ, YangM, BaiY, GeF, WangS. Antioxidant-related catalase CTA1 regulates development, aflatoxin biosynthesis, and virulence in pathogenic fungus aspergillus flavus. Environ Microbiol, 2020, 22(7):2792-2810
CrossRef Google scholar
[45]
Michán S, Lledías F, Baldwin JD, Natvig DO, Hansberg W (2002) Regulation and oxidation of two large monofunctional catalases. Free Radic Biol Med 33(4):521-32. https://doi.org/10.1016/s0891-5849(02)00909-7
[46]
Paris S, Wysong D, Debeaupuis JP, Shibuya K, Philippe B, Diamond RD, Latgé JP (2003) Catalases of Aspergillus fumigatus. Infect Immun 71(6):3551-62. https://doi.org/10.1128/IAI.71.6.3551-3562.2003
[47]
Huai B, Yang Q, Qian YR, Qian WH, Kang ZS, Li J (2019) ABA-Induced Sugar Transporter TaSTP6 Promotes Wheat Susceptibility to Stripe Rust. Plant Physiol 181(3):1328-43. https://doi.org/10.1104/pp.19.00632
[48]
Yin W, Wang, Y, Chen T, Lin Y, Luo C (2018) Functional Evaluation of the Signal Peptides of Secreted Proteins. Bio Protoc 8(9):e2839. https://doi.org/10.21769/BioProtoc.2839
[49]
Longo VD, Gralla EB, Valentine JS (1996) Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae: Mitochondrial production of toxic oxygen species in vivo. J Biol Chem 271(21):12275-12280. https://doi.org/10.1074/jbc.271.21.12275
Funding
National Natural Science Foundation of China(U2003118); Natural Science Basic Research Plan in Shaanxi Province of China(2020JZ-12); National “111 plan”(BP0719026); Shaanxi Innovation Team Project(2018TD-004)

Accesses

Citations

Detail

Sections
Recommended

/