CitCAT1 and CitCAT2 were cloned and highly expressed in mature leaves. High temperatures up-regulated CitCAT1 expression, while low temperatures and Diversispora versiformis up-regulated CitCAT2 expression, maintaining a low oxidative damage. Catalase (CAT), a tetrameric heme-containing enzyme, removes hydrogen peroxide (H2O2) to maintain low oxidative damage in plants exposed to environmental stress. This study aimed to clone CAT genes from Citrus sinensis cv. "Oita 4" and analyze their expression patterns in response to environmental stress, exogenous abscisic acid (ABA), and arbuscular mycorrhizal fungal inoculation. Two CAT genes, CitCAT1 (NCBI accession: PP067858) and CitCAT2 (NCBI accession: PP061394) were cloned, and the open reading frames of their proteins were 1479 bp and 1539 bp, respectively, each encoding 492 and 512 amino acids predicted to be localized in the peroxisome, with CitCAT1 being a stable hydrophilic protein and CitCAT2 being an unstable hydrophilic protein. The similarity of their amino acid sequences reached 83.24%, and the two genes were distantly related. Both genes were expressed in stems, leaves, flowers, and fruits, accompanied by the highest expression in mature leaves. In addition, CitCAT1 expression was mainly up-regulated by high temperatures (37 °C), exogenous ABA, and PEG stress within a short period of time, whereas CitCAT2 expression was up-regulated by exogenous ABA and low-temperature (4 °C) stress. Low temperatures (0 °C) for 12 h just up-regulated CitCAT2 expression in Diversispora versiformis-inoculated plants, and D. versiformis inoculation up-regulated CitCAT2 expression, along with lower hydrogen peroxide and malondialdehyde levels in mycorrhizal plants at low temperatures. It is concluded that CitCAT2 has an important role in resistance to low temperatures as well as mycorrhizal enhancement of host resistance to low temperatures.

College of Horticulture and Gardening Yangtze University Jingzhou 434025 Hubei China

Department of Biology College of Science Princess Nourah bint Abdulrahman University P O Box 84428 11671 Riyadh Saudi Arabia

Division of Horticultural Science College of Agriculture and Life Sciences Gyeongsang National University Jinju 52725 Republic of Korea

Faculty of Science Department of Chemistry University of Hradec Kralove Hradec Kralove 50003 Czech Republic

Zobrazit více v PubMed

Acevedo A, Scandalios JG (1990) Expression of the catalase and superoxide dismutase genes in mature pollen in maize. Theor Appl Genet 80:705–711 PubMed DOI

Acevedo A, Williamson JD, Scandalios JG (1991) Photoregulation of the Cat2 and Cat3 catalase genes in pigmented and pigment-deficient maize: the circadian regulation of Cat3 is superimposed on its quasi-constitutive expression in maize leaves. Genetics 127(3):601–607 PubMed DOI PMC

Ali S, Tyagi A, Bae H (2023) ROS interplay between plant growth and stress biology: challenges and future perspectives. Plant Physiol Biochem 203:108032 PubMed DOI

Amna M, Guillaume Q, Sejir C, Chaouch S, Vanderauwera S, Breusegem FV, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 15:4197–4220

Anjum NA, Sharma P, Gill SS, Hasanuzzaman M, Khan E, Kachhap K, Mohamed AA, Thangavel P, Devi GD, Vasudhevan P, Sofo A, Khan NA, Misra AN, Lukatkin AS, Singh HP, Pereira E, Tuteja N (2016) Catalase and ascorbate peroxidase-representative H DOI

Bai XM, Dong SW, Yang YN, Song Y, Zhang HG, Li SJ (2019) Cloning and expression analysis of catalase gene (LoCAT1) from Larix olgensis. Bull Bot Res 39:539–546

Barrero-Sicilia C, Silvestre S, Haslam RP, Michaelson LV (2017) Lipid remodelling: Unravelling the response to cold stress in Arabidopsis and its extremophile relative Eutrema salsugineum. Plant Sci 263:194–200 PubMed DOI PMC

Chen HJ, Wu SD, Huang GJ, Shen CY, Afiyanti M, Li WJ, Lin YH (2012) Expression of a cloned sweet potato catalase SPCAT1 alleviates ethephon-mediated leaf senescence and HO elevation. J Plant Physiol 169(1):86–97 PubMed DOI

Chu XT, Fu JJ, Sun YF, Xu YM, Miao YJ, Xu YF, Hu TM (2016) Effect of arbuscular mycorrhizal fungi inoculation on cold stress-induced oxidative damage in leaves of Elymus nutans Griseb. S Afr J Bot 104:21–29 DOI

Ding Y, Yang S (2022) Surviving and thriving: how plants perceive and respond to temperature stress. Dev Cell 57:947–958 PubMed DOI

Drory A, Woodson WR (1992) Molecular cloning and nucleotide sequence of a cDNA encoding catalase from tomato. J Plant Physiol 100:1605 DOI

Du YY, Wang PC, Chen J, Song CP (2008) Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana. J Integr Plant Biol 50(10):1318–1326 PubMed DOI

Duc NH, Csintalan Z, Posta K (2018) Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiol Biochem 132:297–307 PubMed DOI

Furtauer L, Weiszmann J, Weckwerth W, Nägele (2019) Dynamics of plant metabolism during cold acclimation. Int J Mol Sci 20:5411 PubMed DOI PMC

Hajiboland R, Joudmand A, Aliasgharzad N, Tolrá R, Poschenrieder C (2019) Arbuscular mycorrhizal fungi alleviate low-temperature stress and increase freezing resistance as a substitute for acclimation treatment in barley. Crop Past Sci 70(3):218–233 DOI

Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Fujita M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9(8):681 PubMed DOI PMC

Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61(6):1041–1052 PubMed DOI

Hou H, Wang SP, Zhang CQ, Xiang YU, Yan LU, Jia H, Wang J, Ying LI, Shen L (2019) Cloning of Catalase2 (CAT2) gene and study on its expression pattern in Nicotiana tabacum L. Chin Tobacco Sci 40(1):1–8

Iwamoto M, Higo H, Higo K (2000) Differential diurnal expression of rice catalase genes: the 5′-flanking region of CatA is not sufficient for circadian control. Plant Sci 151(1):39–46 DOI

Jiang JL (2016) Physiological response of Hanzhong’s main citrus varieties to low temperature stress. Henan Agric Sci 45(3):106–111

Jiang WX, Ye Q, Wu Z, Zhang QY, Wang LH, Liu XF, Guo DD, Wang XQ, Zhang ZL, He HH, Hu LF (2023) Analysis of CAT gene family and functional identification of OsCAT3 in rice. Genes 14(1):138 PubMed DOI PMC

Joo J, Lee YH, Song SI (2014) Rice CatA, CatB, and CatC are involved in environmental stress response, root growth, and photorespiration, respectively. J Plant Biol 57:375–382 DOI

Lee SH, An CS (2005) Differential expression of three catalase genes in hot pepper (Capsicum annuum L.). Mol Cells 20(2):247‒255

Lewandowska A (2017) Genetic screen of Arabidopsis cat2 suppressor mutants to understand the signaling pathways leading to photorespiratory H DOI

Li Y, Yu WC, Chen YY, Tian WM (2019) Molecular cloning and expression analysis of HbCAT2 in rubber tree (Hevea brasiliensis). Mol Plant Breed 17(21):6993–7002

Li QS, Xie YC, Rahman MM, Hashem A, Abd_Allah EF, Wu QS (2022) Arbuscular mycorrhizal fungi and endophytic fungi activate leaf antioxidant defense system of lane late navel orange. J Fungi 8(3):282 DOI

Li QS, Srivastava AK, Zou YN, Wu QS (2023) Field inoculation responses of arbuscular mycorrhizal fungi versus endophytic fungi on sugar metabolism associated changes in fruit quality of Lane late navel orange. Sci Hortic 308:111587 DOI

Liu XQ, Cheng S, Aroca R, Zou YN, Wu QS (2022) Arbuscular mycorrhizal fungi induce flavonoid synthesis for mitigating oxidative damage of trifoliate orange under water stress. Environ Exp Bot 204:105089 DOI

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 PubMed DOI

Ma J, Sun C, Bai L, Dong R, Yan Y, Yu XC, Li Y (2018) Transcriptome analysis of cucumber roots reveals key cold-resistance genes induced by AM fungi. Plant Mol Biol Rep 36:135–148 DOI

Ma WY, Qin QY, Zou YN, Kuča K, Giri B, Wu QS, Hashem A, Al-Arjani A-BF, Almutairi KF, Abd_Allah EF, Xu YJ (2022) Arbuscular mycorrhiza induces low oxidative burst in drought-stressed walnut through activating antioxidant defense systems and heat shock transcription factor expression. Front Plant Sci 13:1089420 PubMed DOI PMC

Mahmoud LM, Vincent CI, Grosser JW, Dutt M (2021) The response of salt-stressed Valencia sweet orange (Citrus sinensis) to salicylic acid and methyl jasmonate treatments. Plant Physiol Rep 26:137–151 DOI

Matsumura T, Tabayashi N, Kamagata Y, Souma C, Saruyama H (2010) Wheat catalase expressed in transgenic rice can improve tolerance against low temperature stress. Physiol Plant 116(3):317–327 DOI

Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Breusegem FV (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61(15):4197–4220 PubMed DOI

Niewiadomska E, Polzien L, Desel C, Rozpadek P, Miszalski Z, Krupinska K (2009) Spatial patterns of senescence and development-dependent distribution of reactive oxygen species in tobacco (Nicotiana tabacum) leaves. J Plant Physiol 166(10):1057–1068 PubMed DOI

Pasbani B, Salimi A, Aliasgharzad N, Hajiboland R (2020) Colonization with arbuscular mycorrhizal fungi mitigates cold stress through improvement of antioxidant defense and accumulation of protecting molecules in eggplants. Sci Hortic 272:109575 DOI

Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55(1):158–161 DOI

Raza A, Su W, Gao A, Mehmood SS, Hussain MA, Nie WL, Lv Y, Zou XL, Zhang XK (2021) Catalase (CAT) gene family in rapeseed (Brassica napus L.): genome-wide analysis, identification, and expression pattern in response to multiple hormones and abiotic stress conditions. Int J Mol Sci 22(8):4281

Shirani BS, Mohammad M (2020) Arbuscular mycorrhizal fungi inoculation to enhance chilling stress tolerance of watermelon. Gesunde Pflanz 72(2):171–179 DOI

Sudhakar C, Lakshmi A, Giridarakumar S (2001) Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci 161(3):613‒619

Sun M, Han JW, Wang ML, Zhang LP, Zhang X, Guo SL, Yin HB (2021) Identification of the CAT gene family in Chenopodium quinoa. Mol Plant Breed 19:5933–5942

Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66 DOI

Wang W, Cheng YY, Chen DD, Liu D, Hu MJ, Dong J, Zhang XP, Song LR, Shen FF (2019) The catalase gene family in cotton: genome-wide characterization and bioinformatics analysis. Cells 8(2):86 PubMed DOI PMC

Wang Y, Zou YN, Shu B, Wu QS (2023) Deciphering molecular mechanisms regarding enhanced drought tolerance in plants by arbuscular mycorrhizal fungi. Sci Hortic 308:111591 DOI

Xing Y, Jia W, Zhang J (2007) AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H PubMed DOI

Yang L, Zou YN, Tian ZH, Wu QS, Kuča K (2021) Effects of beneficial endophytic fungal inoculants on plant growth and nutrient absorption of trifoliate orange seedlings. Sci Hortic 277:109815 DOI

Zhang F, Zou YN, Wu QS, Kuča K (2020) Arbuscular mycorrhizas modulate rootpolyamine metabolism to enhance drought tolerance of trifoliate orange. Environ Exp Bot 171:103926 DOI

Zhang Y, Zheng L, Yun L, Ji L, Li GH, Ji MC, Shi Y, Zheng X (2022) Catalase (CAT) gene family in wheat (Triticum aestivum L.): evolution, expression pattern and function analysis. Int J Mol Sci 23:542

Zimmermann P, Heinlein C, Orendi G, Zentgraf U (2010) Senescence-specific regulation of catalases in Arabidopsis thaliana (L.) Heynh. Plant Cell Environ 29:1049–1060 DOI

Zou YN, Wu QS, Kuča K (2021) Unravelling the role of arbuscular mycorrhizal fungi in mitigating the oxidative burst of plants under drought stress. Plant Biol 23:50–57 PubMed DOI