Abstract
Key message
Methane-triggered lateral root formation is not only a universal event, but also dependent on l-cysteine desulfhydrase-dependent hydrogen sulfide signaling.
Abstract
Whether or how methane (CH4) triggers lateral root (LR) formation has not been elucidated. In this report, CH4 induction of lateral rooting and the role of hydrogen sulfide (H2S) were dissected in tomato and Arabidopsis by using physiological, anatomical, molecular, and genetic approaches. First, we discovered that CH4 induction of lateral rooting is a universal event. Exogenously applied CH4 not only triggered tomato lateral rooting, but also increased activities of l-cysteine desulfhydrase (DES; a major synthetic enzyme of H2S) and induced endogenous H2S production, and contrasting responses were observed in the presence of hypotaurine (HT; a scavenger of H2S) or dl-propargylglycine (PAG; an inhibitor of DES) alone. CH4-triggered lateral rooting were sensitive to the inhibition of endogenous H2S with HT or PAG. The changes in the transcripts of representative cell cycle regulatory genes, miRNA and its target genes were matched with above phenotypes. In the presence of CH4, Arabidopsis mutant Atdes1 exhibited defects in lateral rooting, compared with the wild-type. Molecular evidence showed that the transcriptional profiles of representative target genes modulated by CH4 in wild-type plants were impaired in Atdes1 mutant. Overall, our data demonstrate the main branch of the DES-dependent H2S signaling cascade in CH4-triggered LR formation.
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References
Álvarez C, Calo L, Romero LC, García I, Gotor C (2010) An O-Acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669. https://doi.org/10.1104/pp.109.147975
Álvarez C, García I, Moreno I, Pérez-Pérez ME, Crespo JL, Romero LC, Gotor C (2012) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24:4621–4634. https://doi.org/10.1105/tpc.112.105403
Baudouin E, poilevey A, Hewage NI, Cochet F, Puyauber J, Baily C (2016) The significance of hydrogen sulfide for Arabidopsis seed germination. Front Plant Sci 7:930. https://doi.org/10.3389/fpls.2016.00930
Bloom AA, Taylor JL, 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. https://doi.org/10.1111/j.1469-8137.2010.03259.x
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. https://doi.org/10.1097/CCM.0b013e31823dae05
Bruhn D, Mikkelsen TN, Øbro J, Willats WGT, Ambus P (2009) Effects of temperature, ultraviolet radiation and pectin methyl esterase on aerobic methane release from plant material. Plant Biol 11:43–48. https://doi.org/10.1111/j.1438-8677.2009.00202.x
Bruhn D, Møller IM, Mikkelsen TN, Ambus P (2012) Terrestrial plant methane production and emission. Physiol Plant 144:201–209. https://doi.org/10.1111/j.1399-3054.2011.01551.x
Bruhn D, Mikkelsen TN, Rolsted MMM, Egsgaard H, Ambus P (2014) Leaf surface wax is a source of plant methane formation under UV radiation and in the presence of oxygen. Plant Biol 16:512–516. https://doi.org/10.1111/plb.12137
Cao ZY, Xuan W, Liu ZY, Li XN, Zhao N, Xu P, Wang Z, Guan RZ, Shen WB (2007) Carbon monoxide promotes lateral root formation in rapeseed. Integr Plant Biol 49:1070–1079. https://doi.org/10.1111/j.1672-9072.2007.00482.x
Cao Z, Duan X, Yao P, Cui W, Cheng D, Zhang J, Jin Q, Chen J, Dai C, Shen W (2017)) Hydrogen gas is involved in auxin-induced lateral root formation by modulating nitric oxide synthesis. Int J Mol Sci 18:2084. https://doi.org/10.3390/ijms18102084
Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inzé D, Sandberg G, Casero PJ, Bennet M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852. https://doi.org/10.1105/tpc.13.4.843
Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171. https://doi.org/10.1016/S1360-1385(03)00051-7
Chen B, Li W, Lv C, Zhao M, Jin H, Jin H, Du J, Zhang L, Tang X (2013) Fluorescent probe for highly selective and sensitive detection of hydrogen sulfide in living cells and cardiac tissues. Analyst 138:946–951. https://doi.org/10.1039/C2AN36113B
Chen O, Ye Z, Cao Z, Manaenko A, Ning K, Zhai X, Zhang R, Zhang T, Chen X, Liu W, Sun X (2016) Methane attenuates myocardial ischemia injury in rats through anti-oxidative, anti-apoptotic and anti-inflammatory actions. Free Radical Bio Med 90:1–11. https://doi.org/10.1016/j.freeradbiomed.2015.11.017
Chen Z, Xie Y, Gu Q, Zhao G, Zhang Y, Cui W, Xu S, Wang R, Shen W (2017) The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radic Biol Med 108:465–477. https://doi.org/10.1016/j.freeradbiomed.2017.04.009
Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905. https://doi.org/10.1007/s00425-003-1172-7
Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57:581–588. https://doi.org/10.1093/jxb/erj045
Cui W, Qi F, Zhang Y, Cao H, Zhang J, Wang R, Shen W (2015) Methane-rich water induces cucumber adventitious rooting through heme oxygenase1/carbon monoxide and Ca2+ pathways. Plant Cell Rep 34:435–445. https://doi.org/10.1007/s00299-014-1723-3
Cui W, Cao H, Yao P, Pan J, Gu Q, Xu S, Wang R, Ouyang Z, Wang Q, Shen W (2017) Methane enhances aluminum resistance in alfalfa seedlings by reducing aluminum accumulation and reestablishing redox homeostasis. Biometals 30:719–732. https://doi.org/10.1007/s10534-017-0040-z
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. https://doi.org/10.1016/j.plaphy.2013.12.024
García-Mata C, Lamattina L (2010)) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signaling. New Phytol 188:977–984. https://doi.org/10.1111/j.1469-8137.2010.03465.x
Ghyczy M, Torday C, Kaszaki J, Szabó A, Czóbel M, Boros M (2008) Hypoxia-induced generation of methane in mitochondria and eukaryotic cells-an alternative approach to methanogenesis. Cell Physiol Biochem 21:251–258. https://doi.org/10.1159/000113766
Gu Q, Chen Z, Cui W, Zhang Y, Hu H, Yu X, Wang Q, Shen W (2018) Methane alleviates alfalfa cadmium toxicity via decreasing cadmium accumulation and reestablishing glutathione homeostasis. Ecotoxicol Environ Saf 147:861–871. https://doi.org/10.1016/j.ecoenv.2017.09.054
Guo H, Xiao T, Zhou H, Xie Y, Shen W (2016) Hydrogen sulfide: a versatile regulator of environmental stress in plants. Acta Physiol Plant 38:1–13. https://doi.org/10.1007/s11738-015-2038-x
Guo H, Zhou H, Zhang J, Guan W, Xu S, Shen W, Xu G, Xie Y, Foyer CH (2017)) l-cysteine desulfhydrase-related H2S production is involved in OsSE5-promoted ammonium tolerance in roots of Oryza sativa. Plant Cell Environ 40:1777–1790. https://doi.org/10.1111/pce.12982
Han B, Duan X, Wang Y, Zhu K, Zhang J, Wang R, Hu H, Qi F, Pan J, Yan Y, Shen W (2017) Methane protects against polyethylene glycol-induced osmotic stress in maize by improving sugar and ascorbic acid metabolism. Sci Rep UK 7:46185. https://doi.org/10.1038/srep46185
He F, Xu C, Fu X, Shen Y, Guo L, Leng M, Luo K (2018) The MicroRNA390/TRANS-ACTING SHORT INTERFERING RNA3 module mediates lateral root growth under salt stress via the auxin pathway. Plant Physiol 177:775–791. https://doi.org/10.1104/pp.17.01559
Henneberg A, Sorrell BK, Brix H (2012) Internal methane transport through Juncus effusus: experimental manipulation of morphological barriers to test above- and below-ground diffusion limitation. New Phytol 196:799–806. https://doi.org/10.1111/j.1469-8137.2012.04303.x
Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351. https://doi.org/10.1105/tpc.004960
Jia Y, Li Z, Liu C, Zhang J (2018) Methane medicine: a rising star gas with powerful anti-inflammation, antioxidant, and antiapoptosis properties. Oxid Med Cell Longev 2018:1912746. https://doi.org/10.1155/2018/1912746
Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486. https://doi.org/10.1016/j.bbrc.2011.09.090
Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46. https://doi.org/10.1016/j.plaphy.2012.10.017
Joabsson A, Christensen TR (2001) Methane emissions from wetlands and their relationship with vascular plants: an Arctic example. Global Change Biol 7:919–932. https://doi.org/10.1046/j.1354-1013.2001.00044.x
Keppler F, Hamilton JTG, Braß M, Röckmann T (2006) Methane emissions from terrestrial plants under aerobic conditions. Nature 439:187–191. https://doi.org/10.1038/nature04420
Keppler F, Boros M, Frankenberg C, Lelieveld J, McLeod A, Pirttilä AM, Röckmann T, Schnitzler JP (2009) Methane formation in aerobic environments. Environ Chem 6:459–465. https://doi.org/10.1071/EN09137
Kou N, Xiang Z, Cui W, Li L, Shen W (2018)) Hydrogen sulfide acts downstream of methane to induce cucumber adventitious root development. J Plant Physiol 228:113–120. https://doi.org/10.1016/j.jplph.2018.05.010
Lee HW, Kim NY, Lee DJ, Kim J (2009) LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7. and ARF19 in Arabidopsis. Plant Physiol 151:1377–1389. https://doi.org/10.1104/pp.109.143685
Lenhart K, Bunge M, Ratering S, Neu TR, Schüttmann I, Greule M, Kammann C, Schnell S, Müller C, Zorn H, Keppler F (2012) Evidence for methane production by saprotrophic fungi. Nat Commun 3:1046. https://doi.org/10.1038/ncomms2049
Li L, Wang Y, Shen W (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25:617–631. https://doi.org/10.1007/s10534-012-9551-9
Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013) Hydrogen sulfide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36:1564–1572. https://doi.org/10.1111/pce.12092
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. https://doi.org/10.1007/s00344-012-9262-z
Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signaling molecule? Plant Cell Environ 36:1607–1616. https://doi.org/10.1111/pce.12073
Liu W, Wang D, Tao H, Sun X (2012) Is methane a new therapeutic gas? Med Gas Res 2:25. https://doi.org/10.1186/2045-9912-2-25
Liu D, Xu S, Hu H, Pan J, Li P, Shen W (2017) Endogenous hydrogen sulfide homeostasis is responsible for the alleviation of senescence of postharvest daylily flower via increasing antioxidant capacity and maintained energy status. J Agric Food Chem 65:718–726. https://doi.org/10.1021/acs.jafc.6b04389
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Ma F, Wang L, Li J, Samma MK, Xie Y, Wang R, Wang J, Zhang J, Shen W (2014) Interaction between HY1 and H2O2 in auxin-induced lateral root formation in Arabidopsis. Plant Mol Biol 85:49–61. https://doi.org/10.1007/s11103-013-0168-3
Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375. https://doi.org/10.1105/tpc.105.031716
Manzano C, Pallero-Baena M, Casimiro I, De Rybel B, Orman-Ligeza B, Van Isterdael G, Beeckman T, Draye X, Casero P, del Pozo JC (2014) The emerging role of reactive oxygen species signaling during root development. Plant Physiol 165:1105–1119. https://doi.org/10.1104/pp.114.238873
Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22:1104–1117. https://doi.org/10.1105/tpc.109.072553
Markham JE, Molino D, Gissot L, Bellec Y, Hématy K, Marion J, Belcram K, Palauqui JC, Satiat-JeuneMaître B, Faure JD (2011) Sphingolipids containing very-long-chain fatty acids define a secretory pathway for specific polar plasma membrane protein targeting in Arabidopsis. Plant Cell 23:2362–2378. http://www.plantcell.org/content/23/6/2362
McLeod AR, Fry SC, Loake GJ, Messenger DJ, Reay DS, Smith KA, Yun BW (2008) Ultraviolet radiation drives methane emissions from terrestrial plant pectins. New Phytol 180:124–132. https://doi.org/10.1111/j.1469-8137.2008.02571.x
Mei Y, Chen H, Shen W, Shen W, Huang L (2017)) Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings. BMC Plant Biol 17:162. https://doi.org/10.1186/s12870-017-1110-7
Meng Y, Ma X, Chen D, Wu P, Chen M (2010) MicroRNA-mediated signaling involved in plant root development. Biochem Biophys Res Commun 393:345–349. https://doi.org/10.1016/j.bbrc.2010.01.129
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. https://doi.org/10.1111/j.1365-3040.2008.01892.x
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130. https://doi.org/10.1105/tpc.106.047761
Olas B (2015) Hydrogen sulfide in signaling pathways. Clin Chim Acta 439:212–218. https://doi.org/10.1016/j.cca.2014.10.037
Orman-Ligeza B, Parizot B, de Rycke R, Fernandez A, Himschoot E, Van Breusegem F, Bennett MJ, Périlleux C, Beeckman T, Draye X (2016) RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis. Development 143:3328–3339. https://doi.org/10.1242/dev.136465
Qi F, Xiang Z, Kou N, Cui W, Xu D, Wang R, Zhu D, Shen W (2017) Nitric oxide is involved in methane-induced adventitious root formation in cucumber. Physiol Plant 159:366–377. https://doi.org/10.1111/ppl.12531
Samma MK, Zhou H, Cui W, Zhu K, Zhang J, Shen W (2017) Methane alleviates copper-induced seed germination inhibition and oxidative stress in Medicago sativa. Biometals 30:97–111. https://doi.org/10.1016/j.cca.2014.10.037
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73
Schnittger A, Weinl C, Bouyer D, Schobinger U, Hulskamp M (2003) Misexpression of the cyclin-dependent kinase inhibitor ICK1/KRP1 in single-celled Arabidopsis trichomes reduces endoreduplication and cell size and induces cell death. Plant Cell 15:303–315. https://doi.org/10.1105/tpc.008342
Scuffi D, Álvarez C, Laspina N, Gotor C, Lamattina L, García-Mata C (2014) Hydrogen sulfide generated by l-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol 166:2065–2076. https://doi.org/10.1104/pp.114.245373
Scuffi D, Nietzel T, Di Fino LM, Meyer AJ, Lamattina L, Schwarzländer M, Laxalt AM, García-Mata C (2018) Hydrogen sulfide increases production of NADPH oxidase-dependent hydrogen peroxide and phospholipase D-derived phosphatidic acid in guard cell signaling. Plant Physiol 176:2532–2542. https://doi.org/10.1104/pp.17.01636
Shen J, Xing T, Yuan H, Liu Z, Jin Z, Zhang L, Pei Y (2013) Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions. PLoS ONE 8:e77047. https://doi.org/10.1371/journal.pone.0077047
Shi H, Ye T, Han N, Bian H, Liu X, Chan Z (2015) Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis. J Integr Plant Biol 57:628–640. https://doi.org/10.1111/jipb.12302
Song K, Zhang M, Hu J, Liu Y, Liu Y, Wang Y, Ma X (2015) Methane-rich saline attenuates ischemia/reperfusion injury of abdominal skin flaps in rats via regulating apoptosis level. BMC Surg 15:92. https://doi.org/10.1186/s12893-015-0075-4
Su J, Hu C, Yan X, Jin Y, Chen Z, Guan Q, Wang Y, Zhong D, Jansson C, Wang F, Schnürer A, Sun C (2015)) Expression of barley SUSIBA2 transcription factor yields high-starch low-methane rice. Nature 523:602–606. https://doi.org/10.1038/nature14673
Visser EJW, Nabben RHM, Blom CWPM, Voesenek LACJ (1997)) Elongation by primary lateral roots and adventitious roots during conditions of hypoxia and high ethylene concentrations. Plant Cell Environ 20:647–653. https://doi.org/10.1111/j.1365-3040.1997.00097.x
Wang R (2014) Gasotransmitters: growing pains and joys. Trends Biochem Sci 39:227–232. https://doi.org/10.1016/j.tibs.2014.03.003
Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216. https://doi.org/10.1105/tpc.105.033076
Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119. https://doi.org/10.1007/s11104-011-0936-2
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. https://doi.org/10.1016/j.earscirev.2013.10.001
Wu J, Wang R, Ye Z, Sun X, Chen Z, Xia F, Sun Q, Liu L (2015) Protective effects of methane-rich saline on diabetic retinopathy via anti-inflammation in a streptozotocin-induced diabetic rat model. Biochem Biophys Res Commun 466:155–161. https://doi.org/10.1016/j.bbrc.2015.08.121
Xie Y, Lai D, Mao Y, Zhang W, Shen W, Guan R (2013) Molecular cloning, characterization, and expression analysis of a novel gene encoding l-cysteine desulfhydrase from Brassica napus. Mol Biotechnol 54:737–746. https://doi.org/10.1007/s12033-012-9621-9
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. https://doi.org/10.1104/pp.114.237925
Xu S, Jiang Y, Cui W, Jin Q, Zhang Y, Bu D, Fu J, Wang R, Zhou F, Shen W (2017) Hydrogen enhances adaptation of rice seedlings to cold stress via the reestablishment of redox homeostasis mediated by miRNA expression. Plant Soil 414:53–67. https://doi.org/10.1007/s11104-016-3106-8
Ye Z, Chen O, Zhang R, Nakao A, Fan D, Zhang T, Gu Z, Tao H, Sun X (2015) Methane attenuates hepatic ischemia/reperfusion injury in rats through antiapoptotic, anti-inflammatory, and antioxidative actions. Shock 44:181–187. https://doi.org/10.1097/SHK.0000000000000385
Yin Z, Li C, Han X, Shen F (2008) Identification of conserved microRNAs and their target genes in tomato (Lycopersicon esculentum). Gene 414:60–66. https://doi.org/10.1016/j.gene.2008.02.007
Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094. https://doi.org/10.1111/j.1744-7909.2009.00885.x
Zhu K, Cui W, Dai C, Wu M, Zhang J, Zhang Y, Xie Y, Shen W (2016a) Methane-rich water alleviates NaCl toxicity during alfalfa seed germination. Environ Exp Bot 129:37–47. https://doi.org/10.1016/j.envexpbot.2015.11.013
Zhu D, Mei Y, Shi Y, Hu D, Ren Y, Gu Q, Shen W, Chen X, Xu L, Huang L (2016b) Involvement of glutathione in β-cyclodextrin-hemin complex-induced lateral root formation in tomato seedlings. J Plant Physiol 204:92–100. https://doi.org/10.1016/j.jplph.2016.07.015
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This work was supported by the Natural Science Foundation of Jiangsu Province of China (BK20181317), the National Key Research and Development Plan (2016YFD0101306), the Fundamental Research Funds for the Central Universities (KYTZ201402), the National Natural Science Foundation of China (31772292), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
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YM, YZ, XJ, RW, NX, JH, LH and WS planned and designed the research; YM, YZ, XJ, RW, NX, JH, LH and RG performed experiments; YM, YZ, XJ, RW, NX, JH, RG and WS analysed data; YM, YZ, RW, LH, RG and WS wrote the manuscript.
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Mei, Y., Zhao, Y., Jin, X. et al. l-Cysteine desulfhydrase-dependent hydrogen sulfide is required for methane-induced lateral root formation. Plant Mol Biol 99, 283–298 (2019). https://doi.org/10.1007/s11103-018-00817-3
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DOI: https://doi.org/10.1007/s11103-018-00817-3