Abstract
Key message
Five PeAOX genes from Moso bamboo genome were identified. PeAOX1b_2 -OE improved tolerance to drought and salinity stress in Arabidopsis , indicating it is involved in positive regulation of abiotic stress response.
Abstract
Mitochondrial alternative oxidase (AOX), the important respiratory terminal oxidase in organisms, catalyzes the energy wasteful cyanide (CN)-resistant respiration, which can improve abiotic stresses tolerance and is considered as one of the functional markers for plant resistance breeding. Here, a total of five putative AOX genes (PeAOXs) were identified and characterized in a monocotyledonous woody grass Moso bamboo (Phyllostachys edulis). Phylogenetic analysis revealed that PeAOXs belonged to AOX1 subfamily, and were named PeAOX1a_1, PeAOX1a_2, PeAOX1b_1, PeAOX1b_2 and PeAOX1c, respectively. Evolutionary and divergence patterns analysis revealed that the PeAOX, OsAOX, and BdAOX families experienced positive purifying selection and may have undergone a large-scale duplication event roughly 1.35–155.90 million years ago. Additionally, the organ-specific expression analysis showed that 80% of PeAOX members were mainly expressed in leaf. Promoter sequence analysis of PeAOXs revealed cis-acting regulatory elements (CAREs) responding to abiotic stress. Most PeAOX genes were significantly upregulated after methyl jasmonate (MeJA) and abscisic acid (ABA) treatment. Moreover, under salinity and drought stresses, the ectopic overexpression of PeAOX1b_2 in Arabidopsis enhanced seed germination and seedling establishment, increased the total respiratory rate and the proportion of AOX respiratory pathway in leaf, and enhanced antioxidant ability, suggesting that PeAOX1b_2 is crucial for abiotic stress resistance in Moso bamboo.
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Data availability
The datasets of the current research are presented in the main manuscript and supplementary information file.
References
Borecky J, Nogueira FTS, de Oliveira KAP, Maia IG, Vercesi AE, Arruda P (2006) The plant energy-dissipating mitochondrial systems: depicting the genomic structure and the expression profiles of the gene families of uncoupling protein and alternative oxidase in monocots and dicots. J Exp Bot 57:849–864. https://doi.org/10.1093/jxb/erj070
Bowers JE, Chapman BA, Rong JK, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438. https://doi.org/10.1038/nature01521
Brini F, Hanin M, Lumbreras V, Amara I, Khoudi H, Hassairi A, Pages M, Masmoudi K (2007) Overexpression of wheat dehydrin DHN-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana. Plant Cell Rep 26:2017–2026. https://doi.org/10.1007/s00299-007-0412-x
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10. https://doi.org/10.1186/1471-2229-4-10
Cavalcanti JHF, Oliveira GM, Saraiva KDD, Torquato JPP, Maia IG, de Melo DF, Costa JH (2013) Identification of duplicated and stress-inducible Aox2b gene co-expressed with Aox1 in species of the Medicago genus reveals a regulation linked to gene rearrangement in leguminous genomes. J Plant Physiol 170:1609–1619. https://doi.org/10.1016/j.jplph.2013.06.012
Challabathula D, Analin B, Mohanan A, Bakka K (2022) Differential modulation of photosynthesis, ROS and antioxidant enzyme activities in stress-sensitive and -tolerant rice cultivars during salinity and drought upon restriction of COX and AOX pathways of mitochondrial oxidative electron transport. J Plant Physiol 268:153583. https://doi.org/10.1016/j.jplph.2021.153583
Cheng D, Gao H, Zhang L (2020) Upregulation of mitochondrial alternative oxidase pathway protects photosynthetic apparatus against photodamage under chilling stress in Rumex K-1 leaves. Photosynthetica 58:1116–1121. https://doi.org/10.32615/ps.2020.060
Chien LF, Wu YC, Chen HP (2011) Mitochondrial energy metabolism in young bamboo rhizomes from Bambusa oldhamii and Phyllostachys edulis during shooting stage. Plant Physiol Bioch 49:449–457. https://doi.org/10.1016/j.plaphy.2011.01.024
Clifton R, Lister R, Parker KL, Sappl PG, Elhafez D, Millar AH, Day DA, Whelan J (2005) Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol Biol 58:193–212. https://doi.org/10.1007/s11103-005-5514-7
Clifton R, Millar AH, Whelan J (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. BBA-Bioenergetics 1757:730–741. https://doi.org/10.1016/j.bbabio.2006.03.009
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Considine MJ, Holtzapffel RC, Day DA, Whelan J, Millar AH (2002) Molecular distinction between alternative oxidase from monocots and dicots. Plant Physiol 129:949–953. https://doi.org/10.1104/pp.004150
Costa JH, Mota EF, Cambursano MV, Lauxmann MA, de Oliveira LMN, Lima MDS, Orellano EG, de Melo DF (2010) Stress-induced co-expression of two alternative oxidase (VuAox1 and 2b) genes in Vigna unguiculata. J Plant Physiol 167:561–570. https://doi.org/10.1016/j.jplph.2009.11.001
Costa JH, McDonald AE, Arnholdt-Schmitt B, de Melo DF (2014) A classification scheme for alternative oxidases reveals the taxonomic distribution and evolutionary history of the enzyme in angiosperms. Mitochondrion 19:172–183. https://doi.org/10.1016/j.mito.2014.04.007
Costa JH, dos Santos CP, de Sousa EB, Moreira Netto AN, da Cruz Saraiva KD, Arnholdt-Schmitt B (2017) In silico identification of alternative oxidase 2 (AOX2) in monocots: a new evolutionary scenario. J Plant Physiol 210:58–63. https://doi.org/10.1016/j.jplph.2016.12.009
Cvetkovska M, Vanlerberghe GC (2012) Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytol 195:32–39. https://doi.org/10.1111/j.1469-8137.2012.04166.x
Dahal K, Martyn GD, Vanlerberghe GC (2015) Improved photosynthetic performance during severe drought in Nicotiana tabacum overexpressing a nonenergy conserving respiratory electron sink. New Phytol 208:382–395. https://doi.org/10.1111/nph.13479
Del-Saz NF, Florez-Sarasa I, Clemente-Moreno MJ, Mhadhbi H, Flexas J, Fernie AR, Ribas-Carbo M (2016) Salinity tolerance is related to cyanide-resistant alternative respiration in Medicago truncatula under sudden severe stress. Plant Cell Environ 39:2361–2369. https://doi.org/10.1111/pce.12776
Demircan N, Cucun G, Uzilday B (2020) Mitochondrial alternative oxidase (AOX1a) is required for the mitigation of arsenic-induced oxidative stress in Arabidopsis thaliana. Plant Biotechnol Rep 14:235–245. https://doi.org/10.1007/s11816-020-00595-9
Ding CQ, Chen CT, Su N, Lyu WH, Yang JH, Hu ZY, Zhang MF (2021) Identification and characterization of a natural SNP variant in ALTERNATIVE OXIDASE gene associated with cold stress tolerance in watermelon. Plant Sci 304:110735. https://doi.org/10.1016/j.plantsci.2020.110735
Djajanegara I, Finnegan PM, Mathieu C, McCabe T, Whelan J, Day DA (2002) Regulation of alternative oxidase gene expression in soybean. Plant Mol Biol 50:735–742. https://doi.org/10.1023/a:1019942720636
Fan CJ, Ma JM, Guo QR, Li XT, Wang H, Lu MZ (2013) Selection of reference genes for quantitative real-time PCR in bamboo (Phyllostachys edulis). PLoS ONE 8:e56573. https://doi.org/10.1371/journal.pone.0056573
Feng HQ, Guan DD, Sun K, Wang YF, Zhang TG, Wang RF (2013) Expression and signal regulation of the alternative oxidase genes under abiotic stresses. Acta Bioch Bioph Sin 45:985–994. https://doi.org/10.1093/abbs/gmt094
Finkelstein R (2013) Abscisic acid synthesis and response. Arabidopsis Book 11:e0166. https://doi.org/10.1199/tab.0166
Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer ELL, Bateman A (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251. https://doi.org/10.1093/nar/gkj149
Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer ELL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Res 36:D281–D288. https://doi.org/10.1093/nar/gkm960
Finnegan PM, Whelan J, Millar AH, Zhang Q, Smith MK, Wiskich JT, Day DA (1997) Differential expression of the multigene family encoding the soybean mitochondrial alternative oxidase. Plant Physiol 114:455–466. https://doi.org/10.1104/pp.114.2.455
Florez-Sarasa I, Flexas J, Rasmusson AG, Umbach AL, Siedow JN, Ribas-Carbo M (2011) In vivo cytochrome and alternative pathway respiration in leaves of Arabidopsis thaliana plants with altered alternative oxidase under different light conditions. Plant Cell Environ 34:1373–1383. https://doi.org/10.1111/j.1365-3040.2011.02337.x
Fung RWM, Wang CY, Smith DL, Gross KC, Tian MS (2004) MeSA and MeJA increase steady-state transcript levels of alternative oxidase and resistance against chilling injury in sweet peppers (Capsicum annuum L.). Plant Sci 166:711–719. https://doi.org/10.1016/j.plantsci.2003.11.009
Gandin A, Duffes C, Day DA, Cousins AB (2012) The absence of alternative oxidase AOX1A Results in altered response of photosynthetic carbon assimilation to increasing CO2 in Arabidopsis thaliana. Plant Cell Physiol 53:1627–1637. https://doi.org/10.1093/pcp/pcs107
Gao Y, Wang K, Wang R, Wang L, Liu H, Wu M, Xiang Y (2021) Identification and expression analysis of LBD genes in Moso bamboo (Phyllostachys edulis). J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10475-3
Garmash EV (2021) Role of mitochondrial alternative oxidase in the regulation of cellular homeostasis during development of photosynthetic function in greening leaves. Plant Biol 23:221–228. https://doi.org/10.1111/plb.13217
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioche 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Gu ZL, Steinmetz LM, Gu X, Scharfe C, Davis RW, Li WH (2003) Role of duplicate genes in genetic robustness against null mutations. Nature 421:63–66. https://doi.org/10.1038/nature01198
Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Hereditas 29:1023–1026. https://doi.org/10.1360/yc-007-1023
He Q, Jones DC, Li W, Xie F, Ma J, Sun R, Wang Q, Zhu S, Zhang B (2016) Genome-wide identification of R2R3-MYB genes and expression analyses during abiotic stress in Gossypium raimondii. Sci Rep 6:22980. https://doi.org/10.1038/srep22980
Hou LD, Zhao MR, Huang CY, Wu XL, Zhang JX (2020) Nitric oxide improves the tolerance of Pleurotus ostreatus to heat stress by inhibiting mitochondrial aconitase. Appl Environ Microb 86:e02303-e2319. https://doi.org/10.1128/aem.02303-19
Hou L, Zhao M, Huang C, He Q, Zhang L, Zhang J (2021) Alternative oxidase gene induced by nitric oxide is involved in the regulation of ROS and enhances the resistance of Pleurotus ostreatus to heat stress. Microb Cell Fact 20:137. https://doi.org/10.1186/s12934-021-01626-y
Huang X, von Rad U, Durner J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215:914–923. https://doi.org/10.1007/s00425-002-0828-z
Huang SB, Van Aken O, Schwarzlander M, Belt K, Millar AH (2016) The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants. Plant Physiol 171:1551–1559. https://doi.org/10.1104/pp.16.00166
Hurst LD (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 18:486. https://doi.org/10.1016/s0168-9525(02)02722-1
Ito Y, Saisho D, Nakazono M, Tsutsumi N, Hirai A (1997) Transcript levels of tandem-arranged alternative oxidase genes in rice are increased by low temperature. Gene 203:121–129. https://doi.org/10.1016/s0378-1119(97)00502-7
Juretic N, Hoen DR, Huynh ML, Harrison PM, Bureau TE (2005) The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res 15:1292–1297. https://doi.org/10.1101/gr.4064205
Karpova OV, Kuzmin EV, Elthon TE, Newton KJ (2002) Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell 14:3271–3284. https://doi.org/10.1105/tpc.005603
Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858. https://doi.org/10.1038/nprot.2015.053
Kumari A, Singh P, Kaladhar VC, Bhatoee M, Paul D, Pathak PK, Gupta KJ (2021) Phytoglobin-NO cycle and AOX pathway play a role in anaerobic germination and growth of deepwater rice. Plant Cell Environ 45:178–190. https://doi.org/10.1111/pce.14198
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327. https://doi.org/10.1093/nar/30.1.325
Li CR, Liang DD, Li J, Duan YB, Li H, Yang YC, Qin RY, Li L, Wei PC, Yang JB (2013) Unravelling mitochondrial retrograde regulation in the abiotic stress induction of rice ALTERNATIVE OXIDASE 1 genes. Plant Cell Environ 36:775–788. https://doi.org/10.1111/pce.12013
Liu RH, Meng JL (2003) MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Hereditas 25:317–321
Liu HL, Ww M, Li F, Gao YM, Chen F, Xiang Y (2018) TCP transcription factors in Moso bamboo (Phyllostachys edulis): genome-wide identification and expression analysis. Front Plant Sci 9:1263. https://doi.org/10.3389/fpls.2018.01263
Liu PW, Lyu FF, Zhang YX, Yang Y, Gao ZH, Liang HH, Wei JH (2020) Characterization of AOX family members from Aquilaria sinensis and their responses to wounding. China J Chin Mater Med 45:1641–1647. https://doi.org/10.19540/j.cnki.cjcmm.20200205.107
Liu Y, Yu LL, Peng Y, Geng XX, Xu F (2021) Alternative oxidase inhibition impairs tobacco root development and root hair formation. Front Plant Sci 12:664792. https://doi.org/10.3389/fpls.2021.664792
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lou YF, Sun HY, Li LC, Zhao HS, Gao ZM (2017) Characterization and primary functional analysis of a bamboo ZEP gene from Phyllostachys edulis. DNA Cell Biol 36:747–758. https://doi.org/10.1089/dna.2017.3705
Maxwell DP (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. P Natl Acad Sci USA 96:8271–8276. https://doi.org/10.1073/pnas.96.14.8271
McDonald AE, Vanlerberghe GC, Staples JF (2009) Alternative oxidase in animals: unique characteristics and taxonomic distribution. J Exp Biol 212:2627–2634. https://doi.org/10.1242/jeb.032151
Medentsev AG, Arinbasarova AY, Akimenko VK (1999) Regulation and physiological role of cyanide-resistant oxidases in fungi and plants. Biochemistry 64:1230–1243
Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annu Rev Plant Biol 62:79–104. https://doi.org/10.1146/annurev-arplant-042110-103857
Moller IM (2001) PLANT MITOCHONDRIA AND OXIDATIVE STRESS: Electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Phys 52:561–591. https://doi.org/10.1146/annurev.arplant.52.1.561
Moore RC, Purugganan MD (2003) The early stages of duplicate gene evolution. P Natl Acad Sci USA 100:15682–15687. https://doi.org/10.1073/pnas.2535513100
Moore AL, Umbach AL, Siedow JN (1995) Structure-function relationships of the alternative oxidase of plant mitochondria: a model of the active site. J Bioenerg Biomembr 27:367–377. https://doi.org/10.1007/bf02109999
Nassrallah A, Rougee M, Bourbousse C, Drevensek S, Fonseca S, Iniesto E, Ait-Mohamed O, Deton-Cabanillas AF, Zabulon G, Ahmed I, Stroebel D, Masson V, Lombard B, Eeckhout D, Gevaert K, Loew D, Genovesio A, Breyton C, de Jaeger G, Bowler C, Rubio V, Barneche F (2018) DET1-mediated degradation of a SAGA-like deubiquitination module controls H2Bub homeostasis. Elife 7:e37892. https://doi.org/10.7554/eLife.37892
Navabpour S, Morris K, Allen R, Harrison E, A-H-Mackerness S, Buchanan-Wollaston V. (2003) Expression of senescence-enhanced genes in response to oxidative stress. J Exp Bot 54:2285-2292. https://doi.org/10.1093/jxb/erg267
Nobre T, Campos MD, Lucic-Mercy E, Arnholdt-Schmitt B (2016) Misannotation awareness: a tale of two gene-groups. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00868
Parsons HL, Yip JY, Vanlerberghe GC (1999) Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase. Plant Physiol 121:1309–1320. https://doi.org/10.1104/pp.121.4.1309
Peng ZH, Lu Y, Li LB, Zhao Q, Feng Q, Gao ZM, Lu HY, Hu T, Yao N, Liu KY, Li Y, Fan DL, Guo YL, Li WJ, Lu YQ, Weng QJ, Zhou CC, Zhang L, Huang T, Zhao Y, Zhu CR, Liu XG, Yang XW, Wang T, Miao K, Zhuang CY, Cao XL, Tang WL, Liu GS, Liu YL, Chen J, Liu ZJ, Yuan LC, Liu ZH, Huang XH, Lu TT, Fei BH, Ning ZM, Han B, Jiang ZH (2013) The draft genome of the fast-growing non-timber forest species Moso bamboo (Phyllostachys heterocycla). Nat Genet 45:456–461. https://doi.org/10.1038/ng.2569
Polidoros AN, Mylona PV, Arnholdt-Schmitt B (2009) Aox gene structure, transcript variation and expression in plants. Physiol Plantarum 137:342–353. https://doi.org/10.1111/j.1399-3054.2009.01284.x
Preston JC, Sandve SR (2013) Adaptation to seasonality and the winter freeze. Front Plant Sci 4:167. https://doi.org/10.3389/fpls.2013.00167
Qiao XY, Ruan MJ, Yu T, Cui CY, Chen CY, Zhu YZ, Li FL, Wang SW, Na XF, Wang XM, Bi YR (2022) UCP1 and AOX1a contribute to regulation of carbon and nitrogen metabolism and yield in Arabidopsis under low nitrogen stress. Cell Mol Life Sci. https://doi.org/10.1007/s00018-021-04036-w
Reyes-Diaz M, Lobos T, Cardemil L, Nunes-Nesi A, Retamales J, Jaakola L, Alberdi M, Ribera-Fonseca A (2016) Methyl jasmonate: an alternative for improving the quality and health properties of fresh fruits. Molecules 21:567. https://doi.org/10.3390/molecules21060567
Rhoads DM, McIntosh L (1993) Cytochrome and alternative pathway respiration in tobacco (effects of salicylic acid). Plant Physiol 103:877–883. https://doi.org/10.1104/pp.103.3.877
Saha B, Borovskii G, Panda SK (2016) Alternative oxidase and plant stress tolerance. Plant Signal Behav 11:e1256530. https://doi.org/10.1080/15592324.2016.1256530
Saika H, Ohtsu K, Hamanaka S, Nakazono M, Tsutsumi N, Hirai A (2002) AOX1c, a novel rice gene for alternative oxidase; comparison with rice AOX1a and AOX1b. Genes Genet Syst 77:31–38. https://doi.org/10.1266/ggs.77.31
Saisho D, Nambara E, Naito S, Tsutsumi N, Hirai A, Nakazono M (1997) Characterization of the gene family for alternative oxidase from Arabidopsis thaliana. Plant Mol Biol 35:585–596. https://doi.org/10.1023/a:1005818507743
Schertl P, Braun HP (2014) Respiratory electron transfer pathways in plant mitochondria. Front Plant Sci 5:163. https://doi.org/10.3389/fpls.2014.00163
Sew YS, Stroeher E, Holzmann C, Huang S, Taylor NL, Jordana X, Millar AH (2013) Multiplex micro-respiratory measurements of Arabidopsis tissues. New Phytol 200:922–932. https://doi.org/10.1111/nph.12394
Shiu SH, Karlowski WM, Pan RS, Tzeng YH, Mayer KFX, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234. https://doi.org/10.1105/tpc.020834
Sieger SM, Kristensen BK, Robson CA, Amirsadeghi S, Eng EWY, Abdel-Mesih A, Moller IM, Vanlerberghe GC (2005) The role of alternative oxidase in modulating carbon use efficiency and growth during macronutrient stress in tobacco cells. J Exp Bot 56:1499–1515. https://doi.org/10.1093/jxb/eri146
Soding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21:2144–2144. https://doi.org/10.1093/bioinformatics/bti446
Song C, Zhao Y, Li A, Qi S, Lin Q, Duan Y (2021) Postharvest nitric oxide treatment induced the alternative oxidase pathway to enhance antioxidant capacity and chilling tolerance in peach fruit. Plant Physiol Biochem 167:113–122. https://doi.org/10.1016/j.plaphy.2021.07.036
Su LY, Dai ZW, Li SH, Xin HP (2015) A novel system for evaluating drought-cold tolerance of grapevines using chlorophyll fluorescence. Bmc Plant Biol 15:82. https://doi.org/10.1186/s12870-015-0459-8
Sugie A, Naydenov N, Mizuno N, Nakamura C, Takumi S (2006) Overexpression of wheat alternative oxidase gene Waox1a alters respiration capacity and response to reactive oxygen species under low temperature in transgenic Arabidopsis. Genes Genet Syst 81:349–354. https://doi.org/10.1266/ggs.81.349
Sweetman C, Soole KL, Jenkins CLD, Day DA (2019) Genomic structure and expression of alternative oxidase genes in legumes. Plant Cell Environ 42:71–84. https://doi.org/10.1111/pce.13161
Takumi S, Tomioka M, Eto K, Naydenov N, Nakamura C (2002) Characterization of two non-homoeologous nuclear genes encoding mitochondrial alternative oxidase in common wheat. Genes Genet Syst 77:81–88. https://doi.org/10.1266/ggs.77.81
Taylor NL (2018) Editorial for special issue “plant mitochondria.” Int J Mol Sci 19:3849. https://doi.org/10.3390/ijms19123849
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Van Aken O, Ford E, Lister R, Huang SB, Millar AH (2016) Retrograde signalling caused by heritable mitochondrial dysfunction is partially mediated by ANAC017 and improves plant performance. Plant J 88:542–558. https://doi.org/10.1111/tpj.13276
Vanlerberghe GC, McIntosh L (1992) Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiol 100:115–119. https://doi.org/10.1104/pp.100.1.115
Wang X, Fan P, Song H, Chen X, Li X, Li Y (2009) Comparative proteomic analysis of differentially expressed proteins in shoots of Salicornia europaea under different salinity. J Proteome Res 8:3331–3345. https://doi.org/10.1021/pr801083a
Wang Y, Zhang X (2021) The critical roles of mitochondrial alternative chains in juvenile ark shells (Anadara broughtonii) exposed to acute hypoxia with or without sulfide. Aquat Toxicol 241:105996. https://doi.org/10.1016/j.aquatox.2021.105996
Wang D, Zhang Y, Zhang Z, Zhu J, Yu J (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genom Proteom Bioinf 8:77–80. https://doi.org/10.1016/s1672-0229(10)60008-3
Wu RH, Shi YR, Zhang Q, Zheng WQ, Chen SL, Du L, Lu CF (2019) Genome-wide identification and characterization of the UBP gene family in Moso bamboo (Phyllostachys edulis). Int J Mol Sci 20:4309. https://doi.org/10.3390/ijms20174309
Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139. https://doi.org/10.1046/j.1365-3040.2002.00782.x
Yang HL, Deng LB, Liu HF, Fan SH, Hua W, Liu J (2019) Overexpression of BnaAOX1b confers tolerance to osmotic and salt stress in rapeseed. G3-Genes Genom Genet 9:3501–3511. https://doi.org/10.1534/g3.119.400366
Yang Y, Kang L, Wu RH, Chen YZ, Lu CF (2020) Genome-wide identification and characterization of UDP-glucose dehydrogenase family genes in Moso bamboo and functional analysis of PeUGDH4 in hemicellulose synthesis. Sci Rep 10:10124. https://doi.org/10.1038/s41598-020-67227-8
Yao X, Li JJ, Liu JP, Liu KD (2015) An Arabidopsis mitochondria-localized RRL protein mediates abscisic acid signal transduction through mitochondrial retrograde regulation involving ABI4. J Exp Bot 66:6431–6445. https://doi.org/10.1093/jxb/erv356
Zhang YT, Tang DQ, Lin XC, Ding MQ, Tong ZK (2018) Genome-wide identification of MADS-box family genes in Moso bamboo (Phyllostachys edulis) and a functional analysis of PeMADS5 in flowering. BMC Plant Biol 18:176. https://doi.org/10.1186/s12870-018-1394-2
Zheng WQ, Zhang Y, Zhang Q, Wu RH, Wang XW, Feng SN, Chen SL, Lu CF, Du L (2020) Genome-wide identification and characterization of hexokinase genes in Moso bamboo (Phyllostachys edulis). Front Plant Sci 11:600. https://doi.org/10.3389/fpls.2020.00600
Zhu Y, Wu N, Song W, Yin G, Qin Y, Yan Y, Hu Y (2014) Soybean (Glycine max) expansin gene superfamily origins: segmental and tandem duplication events followed by divergent selection among subfamilies. BMC Plant Biol 14:93
Zhu T, Zou LJ, Li Y, Yao XH, Xu F, Deng XG, Zhang DW, Lin HH (2018) Mitochondrial alternative oxidase-dependent autophagy involved in ethylene-mediated drought tolerance in Solanum lycopersicum. Plant Biotechnol J 16:2063–2076. https://doi.org/10.1111/pbi.12939
Zimmermann P, Zentgraf U (2005) The correlation between oxidative stress and leaf senescence during plant development. Cell Mol Biol Lett 10:515–534
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This research was supported by the National Key Research and Development Program of China (Grant No. 2018 YFD0600101), and the grant for Outstanding Team of Graduate Student Tutors from Beijing Forestry University.
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CL and YC conceptualized the initial study; XW was involved in the experimental layout; XW and XB performed the laboratory experiments; XG and RL helped with bioinformatics analyses; XW drafted the initial article; CL and YC revised the manuscript. All authors read and approved the manuscript.
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Wang, X., Geng, X., Bi, X. et al. Genome-wide identification of AOX family genes in Moso bamboo and functional analysis of PeAOX1b_2 in drought and salinity stress tolerance. Plant Cell Rep 41, 2321–2339 (2022). https://doi.org/10.1007/s00299-022-02923-5
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DOI: https://doi.org/10.1007/s00299-022-02923-5