Abstract
Key message
Methane-rich water triggered adventitious rooting by regulating heme oxygenase1/carbon monoxide and calcium pathways in cucumber explants.
Abstract
Heme oxygenase1/carbon monoxide (HO1/CO) and calcium (Ca2+) were reported as the downstream signals in auxin-induced cucumber adventitious root (AR) formation. Here, we observed that application of methane-rich water (MRW; 80 % saturation) obviously induced AR formation in IAA-depleted cucumber explants. To address the universality, we checked adventitious rooting in soybean and mung bean explants, and found that MRW (50 and 10 % saturation, respectively) exhibited the similar inducing results. To further determine if the HO1/CO system participated in MRW-induced adventitious rooting, MRW, HO1 inducer hemin, its activity inhibitor zinc protoporphyrin IX (ZnPP), and its catalytic by-products CO, bilirubin, and Fe2+ were used to detect their effects on cucumber adventitious rooting in IAA-depleted explants. Subsequent results showed that MRW-induced adventitious rooting was blocked by ZnPP and further reversed by 20 % saturation CO aqueous solution. However, the other two by-products of HO1, bilirubin and Fe2+, failed to induce AR formation. Above responses were consistent with the MRW-induced increases of HO1 transcript and corresponding protein level. Further molecular evidence indicted that expression of marker genes, including auxin signaling-related genes and cell cycle regulatory genes, were modulated by MRW alone but blocked by the cotreatment with ZnPP, the latter of which could be significantly rescued by the addition of CO. By using the Ca2+-channel blocker and Ca2+ chelator, the involvement of Ca2+ pathway in MRW-induced adventitious rooting was also suggested. Together, our results indicate that MRW might serve as a stimulator of adventitious rooting, which was partially mediated by HO1/CO and Ca2+ pathways.
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Abbreviations
- AR:
-
Adventitious root
- ARP:
-
Adventitious root primordium
- BR:
-
Bilirubin
- BV:
-
Biliverdin IX
- CDPK:
-
Calcium-dependent protein kinase
- CH4 :
-
Methane
- CO:
-
Carbon monoxide
- EGTA:
-
Ethylene glycol-bis(2-aminoethylether)-N,N,N′,N′-tetraacetic acid
- HO:
-
Heme oxygenase
- HO1:
-
Heme oxygenase1
- MRW:
-
Methane-rich water
- ZnPP:
-
Zinc protoporphyrin IX
References
Bai X, Todd CD, Desikan R, Yang Y, Hu X (2012) N-3-oxo-decanoyl-L-homoserine-lactone activates auxin-induced adventitious root formation via hydrogen peroxide- and nitric oxide-dependent cyclic GMP signaling in mung bean. Plant Physiol 158:725–736
Bellamine J, Penel C, Greppin H, Gaspar T (1998) Confirmation of the role of auxin and calcium in the late phases of adventitious root formation. Plant Growth Regul 26:191–194
Bilban M, Haschemi A, Wegiel B, Chin BY, Wagner O, Otterbein LE (2008) Heme oxygenase and carbon monoxide initiate homeostatic signaling. J Mol Med (Berl) 86:267–279
Bloom AA, Lee-Taylor J, Madronich S, Messenger DJ, Palmer PI, Reay DS, McLeod AR (2010) Global methane emission estimates from ultraviolet irradiation of terrestrial plant foliage. New Phytol 187:417–425
Boros M, Ghyczy M, Érces D, Varga G, Tőkés T, Kupai K, Torday C, Kaszaki J (2012) The anti-inflammatory effects of methane. Crit Care Med 40:1269–1278
Bruhn D, Mikkelsen TN, Øbro J, Willats WG, Ambus P (2009) Effects of temperature, ultraviolet radiation and pectin methyl esterase on aerobic methane release from plant material. Plant Biol (Stuttg) 11:43–48
Bruhn D, Møller IM, Mikkelsen TN, Ambus P (2012) Terrestrial plant methane production and emission. Physiol Plant 144:201–209
Cao Z, Geng B, Xu S, Xuan W, Nie L, Shen W, Liang Y, Guan R (2011) BnHO1, a haem oxygenase-1 gene from Brassica napus, is required for salinity and osmotic stress-induced lateral root formation. J Exp Bot 62:4675–4689
Chen YH, Chao YY, Hsu YY, Hong CY, Kao CH (2012) Heme oxygenase is involved in nitric oxide- and auxin-induced lateral root formation in rice. Plant Cell Rep 31:1085–1091
Chen YH, Chao YY, Hsu YY, Kao CH (2013) Heme oxygenase is involved in H2O2-induced lateral root formation in apocynin-treated rice. Plant Cell Rep 32:219–226
Cui W, Zhang J, Xuan W, Xie Y (2013) Up-regulation of heme oxygenase-1 contributes to the amelioration of aluminum-induced oxidative stress in Medicago sativa. J Plant Physiol 170:1328–1336
DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signalling. Biochem J 425:27–40
Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620
Drew MC, Jackson MB, Giffard S (1979) Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) in roots may be adaptive responses to flooding in Zea mays L. Planta 147:83–88
Emborg TJ, Walker JM, Noh B, Vierstra RD (2006) Multiple heme oxygenase family members contribute to the biosynthesis of the phytochrome chromophore in Arabidopsis. Plant Physiol 140:856–868
Fang T, Cao Z, Li J, Shen W, Huang L (2014) Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato. Plant Physiol Biochem 76:44–51
He H, He L (2014) Heme oxygenase 1 and abiotic stresses in plants. Acta Physiol Plant 36:581–588
Hsu YY, Chao YY, Kao CH (2013) Methyl jasmonate-induced lateral root formation in rice: the role of heme oxygenase and calcium. J Plant Physiol 170:63–69
Jin Q, Zhu K, Cui W, Xie Y, Han B, Shen W (2013) Hydrogen gas acts as a novel bioactive molecule in enhancing plant tolerance to paraquat-induced oxidative stress via the modulation of heme oxygenase-1 signalling system. Plant Cell Environ 36:956–969
Keppler F, Hamilton JT, Braß M, Röckmann T (2006) Methane emissions from terrestrial plants under aerobic conditions. Nature 439:187–191
Kohli A, Sreenivasulu N, Lakshmanan P, Kumar PP (2013) The phytohormone crosstalk paradigm takes center stage in understanding how plants respond to abiotic stresses. Plant Cell Rep 32:945–957
Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563
Kumar PP (2013) Plant hormones and their intricate signaling networks: unraveling the nexus. Plant Cell Rep 32:731–732
Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351
Lanteri ML, Laxalt AM, Lamattina L (2008) Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiol 147:188–198
Li S, Xue L, Xu S, Feng H, An L (2007) Hydrogen peroxide involvement in formation and development of adventitious roots in cucumber. Plant Growth Regul 52:173–180
Li SW, Xue L, Xu S, Feng H, An L (2009) Mediators, genes and signaling in adventitious rooting. Bot Rev 75:230–247
Li MY, Cao ZY, Shen WB, Cui J (2011) Molecular cloning and expression of a cucumber (Cucumis sativus L.) heme oxygenase-1 gene, CsHO1, which is involved in adventitious root formation. Gene 486:47–55
Li ZG, Gong M, Xie H, Yang L, Li J (2012) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 185–186:185–189
Liao WB, Zhang ML, Huang GB, Yu JH (2012) Ca2+ and CaM are involved in NO- and H2O2-induced adventitious root development in marigold. J Plant Growth Regul 31:253–264
Lin YT, Li MY, Cui WT, Lu W, Shen WB (2012) Haem oxygenase-1 is involved in hydrogen sulfide-induced cucumber adventitious root formation. J Plant Growth Regul 31:519–528
Lin Y, Zhang W, Qi F, Cui W, Xie Y, Shen W (2014) Hydrogen-rich water regulates cucumber adventitious root development in a heme oxygenase-1/carbon monoxide-dependent manner. J Plant Physiol 171:1–8
Messenger DJ, McLeod AR, Fry SC (2009) The role of ultraviolet radiation, photosensitizers, reactive oxygen species and ester groups in mechanisms of methane formation from pectin. Plant Cell Environ 32:1–9
Nisbet RER, Fisher R, Nimmo RH, Bendall DS, Crill PM, Gallego-Sala AV, Hornibrook ERC, López-Juez E, Lowry D, Nisbet PBR, Shuckburgh EF, Sriskantharajah S, Howe CJ, Nisbet EG (2009) Emission of methane from plants. Proc R Soc B 276:1347–1354
Noriega GO, Balestrasse KB, Batlle A, Tomaro ML (2004) Heme oxygenase exerts a protective role against oxidative stress in soybean leaves. Biochem Biophys Res Commun 323:1003–1008
Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956
Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248
Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286
Sahakian AB, Jee SR, Pimentel M (2010) Methane and the gastrointestinal tract. Dig Dis Sci 55:2135–2143
Saini S, Sharma I, Kaur N, Pati PK (2013) Auxin: a master regulator in plant root development. Plant Cell Rep 32:741–757
Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665
Shekhawat GS, Verma K (2010) Haem oxygenase (HO): an overlooked enzyme of plant metabolism and defence. J Exp Bot 61:2255–2270
Simontacchi M, García-Mata C, Bartoli CG, Santa-María GE, Lamattina L (2013) Nitric oxide as a key component in hormone-regulated processes. Plant Cell Rep 32:853–866
Steffens B, Wang J, Sauter M (2006) Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223:604–612
Wang R (2014) Gasotransmitters: growing pains and joys. Trends Biochem Sci 39:227–232
Wang ZP, Chang SX, Chen H, Han XG (2013) Widespread non-microbial methane production by organic compounds and the impact of environmental stresses. Earth-Sci Rev 127:193–202
Wang L, Ma F, Xu S, Zheng T, Wang R, Chen H, Shen W (2014) Cloning and characterization of a heme oxygenase-2 gene from rice (Oryza sativa L.), and its expression analysis in response to some abiotic stresses. Acta Physiol Plant 36:893–902
Wishkerman A, Greiner S, Ghyczy M, Boros M, Rausch T, Lenhart K, Keppler F (2011) Enhanced formation of methane in plant cell cultures by inhibition of cytochrome c oxidase. Plant Cell Environ 34:457–464
Xie Y, Mao Y, Zhang W, Lai D, Wang Q, Shen W (2014) Reactive oxygen species-dependent nitric oxide production contributes to hydrogen-promoted stomatal closure in Arabidopsis. Plant Physiol 165:759–773
Xu S, Zhang B, Cao ZY, Ling TF, Shen WB (2011) Heme oxygenase is involved in cobalt chloride-induced lateral root development in tomato. Biometals 24:181–191
Xuan W, Zhu FY, Xu S, Huang BK, Ling TF, Qi JY, Ye MB, Shen WB (2008) The heme oxygenase/carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process. Plant Physiol 148:881–893
Xuan W, Xu S, Li M, Han B, Zhang B, Zhang J, Lin Y, Huang J, Shen W, Cui J (2012) Nitric oxide is involved in hemin-induced cucumber adventitious rooting process. J Plant Physiol 169:1032–1039
Acknowledgments
This work was supported by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), and the National Natural Science Foundation of China (J1210056 and J1310015).
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The authors declare that they have no conflict of interest.
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Communicated by Chun-Hai Dong.
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Cui, W., Qi, F., Zhang, Y. et al. Methane-rich water induces cucumber adventitious rooting through heme oxygenase1/carbon monoxide and Ca2+ pathways. Plant Cell Rep 34, 435–445 (2015). https://doi.org/10.1007/s00299-014-1723-3
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DOI: https://doi.org/10.1007/s00299-014-1723-3