H2S-mediated balance regulation of stomatal and non-stomatal factors responding to drought stress in Chinese cabbage

Wenze Zhang , Lei Wang , Liping Zhang , Xiangqun Kong , Jiao Zhang , Xin Wang , Yanxi Pei , Zhuping Jin

Horticulture Research ›› 2023, Vol. 10 ›› Issue (3) : 284

PDF (1730KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (3) :284 DOI: 10.1093/hr/uhac284
Article
research-article
H2S-mediated balance regulation of stomatal and non-stomatal factors responding to drought stress in Chinese cabbage
Author information +
History +
PDF (1730KB)

Abstract

Increased evidence has shown that hydrogen sulfide (H2S), a novel gasotransmitter, could enhance drought resistance in plants by inducing stomatal closure, with concurrent enhancement of photosynthetic efficiency, but little is known about the mechanism behind this contradictory phenomenon. This study examined the regulating mechanism of H2S in response to drought stress from stomatal and non-stomatal factors in Chinese cabbage. The results showed that exogenous H2S could increase the accumulation of photosynthetic pigments and alleviate the damage caused by drought stress. It also regulated the expression in transcriptional level and the activity of ribulose 1,5-bisphosphate carboxylase/oxygenase (BrRuBisCO) under drought stress. The large subunit of BrRuBisCO was found to be modified by S-sulfhydration, which might be the reason for its increased enzyme activity. The fluxes of Cl, K+, and H+ in the guard cells were detected by non-invasive micro-test techniques while under drought stress. The results indicated that H2S signaling induced a transmembrane Cl and H+ efflux and inhibited K+ influx, and the Cl channel was the main responders for H2S-regulated stomatal movement. In conclusion, H2S signal not only activated the ion channel proteins located in the guard cell membrane to induce stomatal closure, but also regulated the transcriptional expression and the activity of RuBisCO, a non-stomatal factor to enhance the photosynthetic efficiency of leaves. There is therefore a beneficial balance between the regulation of H2S signaling on stomatal factors and non-stomatal factors due to drought stress, which needs to be better understood to apply it practically to increase crop yields.

Cite this article

Download citation ▾
Wenze Zhang, Lei Wang, Liping Zhang, Xiangqun Kong, Jiao Zhang, Xin Wang, Yanxi Pei, Zhuping Jin. H2S-mediated balance regulation of stomatal and non-stomatal factors responding to drought stress in Chinese cabbage. Horticulture Research, 2023, 10 (3) : 284 DOI:10.1093/hr/uhac284

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was funded by the National Natural Science Foundation of China (32172550 and 31972428), Shanxi Province Natural Science Foundation (20210302123431), and Research Project Supported by Shanxi Scholarship Council of China (2020-014). We thank International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript.

Author contributions

Y.P. and Z.J. designed research; L.W., W.Z., and X.K. performed experiments; W.Z. and L.Z. analysed data and prepared figures; L.W., W.Z., Y.P., and Z.J. drafted, edited, and revised manuscript; Y.P. and Z.J. approved the final version of the manuscript.

Data availability

All relevant data can be found in the manuscript and supplementary materials.

Conflict of interests

The authors declare no conflict of interest.

References

[1]

Chen LS, Liu XH . Effects of water stress on some enzyme activities related to respiratory metabolism in litchi chinensis leaves. Sci Silvae Sin. 2003; 39: 39-43.

[2]

Earl HJ . Stomatal and non-stomatal restrictions to carbon assimilation in soybean (glycine max) lines differing in water use efficiency. Environ Exp Bot. 2002; 48: 237-46.

[3]

Dias PC, Araujo WL, Moraes G et al. Morphological and physiological responses of two coffee progenies to soil water availability. J Plant Physiol. 2007; 164: 1639-47.

[4]

Wang J, Li C, Li L et al. Exploitation of drought tolerance-related genes for crop improvement. Int J Mol Sci. 2021; 22: 10265.

[5]

Park BJ, Liu Z, Kanno A et al. Genetic improvement of Chinese cabbage for salt and drought tolerance by constitutive expression of a B. napus LEA gene. Plant Sci. 2005; 169: 553-8.

[6]

Wang R . Gasotransmitters: growing pains and joys. Trends Biochem Sci. 2014; 39: 227-32.

[7]

Gotor C, García I, Aroca Á et al. Signaling by hydrogen sulfide and cyanide through post-translational modification. J Exp Bot. 2019; 70: 4251-65.

[8]

Paul BD, Snyder SH . H2S signalling through protein sulfhydration and beyond . Nat Rev Mol Cell Biol. 2012; 13: 499-507.

[9]

Mustafa AK, Gadalla MM, Sen N et al. H2S signals through protein S-sulfhydration . Sci Signal. 2009; 2: ra72.

[10]

Thakur M, Anand A . Hydrogen sulfide: an emerging signalling molecule regulating drought stress response in plants. Physiol Plant. 2021; 172: 1227-43.

[11]

Shen J, Su Y, Zhou C et al. A putative rice L-cysteine desulfhydrase encodes a true L-cysteine synthase that regulates plant cadmium tolerance. Plant Growth Regul. 2019; 89: 217-26.

[12]

Guo HM, Xiao TY, Zhou H et al. Hydrogen sulfide: a versatile regulator of environmental stress in plants. Acta Physiol Plant. 2016; 38: 16.

[13]

Li ZG, Min X, Zhou ZH . Hydrogen sulfide: a signal molecule in plant cross-adaptation. Front Plant Sci. 2016; 7: 1621.

[14]

Jin ZP, Xue S, Luo Y et al. Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem. 2013; 62: 41-6.

[15]

Jin ZP, Shen J, Qiao Z et al. Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun. 2011; 414: 481-6.

[16]

García-Mata C, Lamattina L . Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol. 2010; 188: 977-84.

[17]

Deng GB, Zhou LJ, Wang YY et al. Hydrogen sulfide acts downstream of jasmonic acid to inhibit stomatal development in Arabidopsis. Planta. 2020; 251: 42.

[18]

Scuffi D, Álvarez C, Laspina N et al. Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol. 2014; 166: 2065-76.

[19]

Liu J, Hou LX, Liu GH et al. Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Chin Sci Bull. 2011; 56: 3547-53.

[20]

Pantaleno R, Scuffi D, García-Mata C . Hydrogen sulphide as a guard cell network regulator. New Phytol. 2020; 230: 451-6.

[21]

Chen J, Zhou H, Xie YJ . SnRK2.6 phosphorylation/persulfidation: where ABA and H2S signaling meet . Trends Plant Sci. 2021; 26: 1207-9.

[22]

Zhou MJ, Zhang J, Shen J et al. Hydrogen sulfide-linked persulfidation of ABI4 controls ABA responses through the transactivation of MAPKKK18 in Arabidopsis. Mol Plant. 2021; 14: 921-36.

[23]

Wang L, Wan RJ, Shi YH et al. Hydrogen sulfide activates S-type anion channel via OST1 and Ca 2+ modules . Mol Plant. 2016; 9: 489-91.

[24]

Papanatsiou M, Scuffi D, Blatt MR et al. Hydrogen sulfide regulates inward-rectifying K + channels in conjunction with stomatal closure . Plant Physiol. 2015; 168: 29-35.

[25]

Jin ZP, Wang Z, Ma Q et al. Hydrogen sulfide mediates ion fluxes inducing stomatal closure in response to drought stress in Arabidopsis thaliana. Plant Soil. 2017; 419: 141-52.

[26]

Caemmerer SV . Rubisco carboxylase/oxygenase: from the enzyme to the globe: a gas exchange perspective. J Plant Physiol. 2020; 252: 153240.

[27]

Portis AR Jr, Parry MA . Discoveries in Rubisco (ribulose 1,5-bisphosphate carboxylase/oxygenase): a historical perspective. Photosynth Res. 2007; 94: 121-43.

[28]

Liu FJ, Fu X, Wu G et al. Hydrogen peroxide is involved in hydrogen sulfide-induced carbon assimilation and photoprotection in cucumber seedlings. Environ Exp Bot. 2020; 175: 104052.

[29]

Chen J, Wu FH, Wang WH et al. Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot. 2011; 62: 4481-93.

[30]

Krantev A, Yordanova R, Janda T et al. Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol. 2008; 165: 920-31.

[31]

Salesse-Smith CE, Sharwood RE, Busch FA et al. Overexpression of Rubisco subunits with RAF1 increases Rubisco content in maize. Nature Plants. 2018; 4: 802-10.

[32]

Lagercrantz U . Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics. 1998; 150: 1217-28.

[33]

Chen S, Jia H, Wang X et al. Hydrogen sulfide positively regulates abscisic acid signaling through persulfidation of SnRK2.6 in guard cells. Mol Plant. 2020; 13: 732-44.

[34]

Shen J, Zhang J, Zhou M et al. Persulfidation-based modification of cysteine desulfhydrase and the NADPH oxidase RBOHD controls guard cell abscisic acid signaling. Plant Cell. 2020; 32: 1000-17.

[35]

Zhou H, Zhang J, Shen J et al. Redox-based protein persulfidation in guard cell ABA signaling. Plant Signal Behav. 2020; 15: 1741987.

[36]

Du XZ, Jin Z, Zhang L et al. H2S is involved in ABA-mediated stomatal movement through MPK4 to alleviate drought stress in Arabidopsis thaliana . Plant Soil. 2019; 435: 295-307.

[37]

Zhang J, Zhou M, Ge Z et al. Abscisic acid-triggered guard cell L-cysteine desulfhydrase function and in situ hydrogen sulfide production contributes to heme oxygenase-modulated stomatal closure. Plant Cell Environ. 2020; 43: 624-36.

[38]

Jezek M, Silva-Alvim FAL, Hills A et al. Guard cell endomembrane Ca 2+-ATPases underpin a ’carbon memory’ of photosynthetic assimilation that impacts on water-use efficiency . Nature Plants. 2021; 7: 1301-13.

[39]

Ward JM, Maser P, Schroeder JI . Plant ion channels: gene families, physiology, and functional genomics analyses. Annu Rev Physiol. 2009; 71: 59-82.

[40]

Blatt MR . Cellular signaling and volume control in stomatal movements in plants. Annu Rev Cell Dev Biol. 2000; 16: 221-41.

[41]

Li HS, ed. Plant Physiological and Biochemical Experiment Principles and Techniques. Beijing: Higher Education Press, 2006.

[42]

Wang ZQ, Mu Y, Hao X et al. H2S aids osmotic stress resistance by S-sulfhydration of melatonin production-related enzymes in Arabidopsis thaliana . Plant Cell Rep. 2022; 41: 365-76.

[43]

Li CF, Li LR . Comparison of the activity of RuBP carboxylase as measured by spectrophotometry and 14C labeling . Plant Physiol Commun. 1989; 1: 49-50.

[44]

Yan S, McLamore ES, Dong S et al. The role of plasma membrane H +-ATPase in jasmonate-induced ion fluxes and stomatal closure in Arabidopsis thaliana . Plant J. 2015; 83: 638-49.

PDF (1730KB)

73

Accesses

0

Citation

Detail

Sections
Recommended

/