Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
Shopping Cart: ( empty )
You are here: Home > Journals > FP > FP19079
RESEARCH ARTICLE
Contents Vol 46(10)

Light regulates hydrogen sulfide signalling during skoto- and photo-morphogenesis in foxtail millet

Zhiqiang Liu A C , Chunyu Cao A C , Yawen Li A C , Guangdong Yang A B C and Yanxi Pei https://orcid.org/0000-0002-8428-3399 A C D
+ Author Affiliations
- Author Affiliations

A School of Life Science, Shanxi University, Taiyuan 030006, China.

B Department of Chemistry and Biochemistry, Laurentian University, Sudbury, ON P3E 2C6, Canada.

C Shanxi Key Laboratory for Research and Development of Regional Plants, Taiyuan 030006, China.

D Corresponding author. Email: peiyanxi@sxu.edu.cn

Functional Plant Biology 46(10) 916-924 https://doi.org/10.1071/FP19079
Submitted: 27 March 2019  Accepted: 27 May 2019   Published: 25 June 2019

Abstract

Signal transduction mediated by photoreceptors regulates many physiological processes during plant growth and development including seed germination, flowering and photosynthesis, which are also regulated by hydrogen sulfide (H2S). However, studies of the connection between the vital environmental factors – light and the significant endogenous gasotransmitter – H2S, is lacking. Here, the seedlings of foxtail millet were used to reveal the mechanism of light regulation in H2S generation. Results showed that seedling hypocotyl elongation was promoted by H2S, but inhibited by HA under dark or white light condition. H2S contents in hypocotyl increased at first under red, blue or white light then decreased, and the duration of increase under white light was longer than under red or blue light. The activity of cysteine desulfhydrases, which catalyse H2S generation, was increased by red light but decreased by blue and white light. The expressions of cysteine desulfhydrases coding genes LCD1 and LCD2 were promoted by red or white light, but inhibited by blue light. In contrast, DES gene was promoted by white light but inhibited by red or blue light. In addition, the activities of LCDs were regulated by the phosphorylation mediated by photoreceptors PHYB and CRY1/CRY2. Finally, there are two pathways of light regulating H2S production, including a rapid process that involves the modification of phosphorylation on LCDs protein mediated by photoreceptors directly or indirectly, as well as a slower process that involves in regulating the expressions of LCDs and DES genes. This discovery has potential value for the application of H2S in agricultural production protecting the crops from unsuited light condition.

Additional keywords: cysteine desulfhydrases, light signalling, phosphorylation, photoreceptor.


References

Al-Sady B, Ni W, Kircher S, Fer ES, Quail PH (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Molecular Cell 23, 439–446.
| Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation.Crossref | GoogleScholarGoogle Scholar | 16885032PubMed |

Alvarez C, Calo L, Romero LC, Garcia I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiology 152, 656–669.
| An O-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19955263PubMed |

Barton L, Newsome SD, Chen F, Wang H, Guilderson TP, Bettinger RL (2009) Agricultural origins and the isotopic identity of domestication in northern China. Proceedings of the National Academy of Sciences of the United States of America 106, 5523–5528.
| Agricultural origins and the isotopic identity of domestication in northern China.Crossref | GoogleScholarGoogle Scholar | 19307567PubMed |

Bauer D, Viczian A, Kircher S, Nobis T, Nitschke R, Kunkel T, Panigrahi KC, Adam E, Fejes E, Schafer E, Nagy F (2004) Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis. The Plant Cell 16, 1433–1445.
| Constitutive photomorphogenesis 1 and multiple photoreceptors control degradation of phytochrome interacting factor 3, a transcription factor required for light signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15155879PubMed |

Bethke G, Unthan T, Uhrig JF, Poschl Y, Gust AA, Scheel D, Lee J (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proceedings of the National Academy of Sciences of the United States of America 106, 8067–8072.
| Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling.Crossref | GoogleScholarGoogle Scholar | 19416906PubMed |

Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annual Review of Genetics 38, 87–117.
| Light signal transduction in higher plants.Crossref | GoogleScholarGoogle Scholar | 15568973PubMed |

Chen J, Wu F, Wang W, Zheng C, Lin G, Dong X, He J, Pei Z, Zheng H (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. Journal of Experimental Botany 62, 4481–4493.
| Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings.Crossref | GoogleScholarGoogle Scholar | 21624977PubMed |

Chung PJ, Park BS, Wang H, Liu J, Jang IC, Chua NH (2016) Light-Inducible MiR163 targets PXMT1 transcripts to promote seed germination and primary root elongation in Arabidopsis. Plant Physiology 170, 1772–1782.

Fang H, Liu Z, Jin Z, Zhang L, Liu D, Pei Y (2016) An emphasis of hydrogen sulfide-cysteine cycle on enhancing the tolerance to chromium stress in Arabidopsis. Environmental Pollution 213, 870–877.
| An emphasis of hydrogen sulfide-cysteine cycle on enhancing the tolerance to chromium stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27038574PubMed |

Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiology 155, 93–100.
| Understanding oxidative stress and antioxidant functions to enhance photosynthesis.Crossref | GoogleScholarGoogle Scholar | 21045124PubMed |

Hirose F, Inagaki N, Hanada A, Yamaguchi S, Kamiya Y, Miyao A, Hirochika H, Takano M (2012) Cryptochrome and phytochrome cooperatively but independently reduce active gibberellin content in rice seedlings under light irradiation. Plant & Cell Physiology 53, 1570–1582.
| Cryptochrome and phytochrome cooperatively but independently reduce active gibberellin content in rice seedlings under light irradiation.Crossref | GoogleScholarGoogle Scholar |

Jiao Y, Lau OS, Deng X (2007) Light-regulated transcriptional networks in higher plants. Nature Reviews. Genetics 8, 217–230.
| Light-regulated transcriptional networks in higher plants.Crossref | GoogleScholarGoogle Scholar | 17304247PubMed |

Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochemical and Biophysical Research Communications 414, 481–486.
| Hydrogen sulfide improves drought resistance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 21986537PubMed |

Krzymuski M, Cerdán PD, Zhu L, Vinh A, Chory J, Huq E, Casal JJ (2014) Phytochrome A antagonizes PHYTOCHROME INTERACTING FACTOR 1 to prevent over-activation of photomorphogenesis. Molecular Plant 7, 1415–1428.
| Phytochrome A antagonizes PHYTOCHROME INTERACTING FACTOR 1 to prevent over-activation of photomorphogenesis.Crossref | GoogleScholarGoogle Scholar | 25009301PubMed |

Lagarias JC, Rapoport H (1980) Chromopeptides from phytochrome. The structure and linkage of the PR form of the phytochrome chromophore. Journal of the American Chemical Society 102, 4821–4828.
| Chromopeptides from phytochrome. The structure and linkage of the PR form of the phytochrome chromophore.Crossref | GoogleScholarGoogle Scholar |

Lata C, Bhutty S, Bahadur RP, Majee M, Prasad M (2011) Association of an SNP in a novel DREB2-like gene SiDREB2 with stress tolerance in foxtail millet (Setaria italica (L.)). Journal of Experimental Botany 62, 3387–3401.
| Association of an SNP in a novel DREB2-like gene SiDREB2 with stress tolerance in foxtail millet (Setaria italica (L.)).Crossref | GoogleScholarGoogle Scholar | 21414959PubMed |

Lazaro A, Mouriz A, Pineiro M, Jarillo JA (2015) Red light-mediated degradation of CONSTANS by the E3 ubiquitin ligase HOS1 regulates photoperiodic flowering in Arabidopsis. The Plant Cell 27, 2437–2454.
| Red light-mediated degradation of CONSTANS by the E3 ubiquitin ligase HOS1 regulates photoperiodic flowering in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 26373454PubMed |

Li F-W, Mathews S (2016) Evolutionary aspects of plant photoreceptors. Journal of Plant Research 129, 115–122.
| Evolutionary aspects of plant photoreceptors.Crossref | GoogleScholarGoogle Scholar | 26843269PubMed |

Li J, Li G, Wang H, Deng X (2011) Phytochrome signaling mechanisms. The Arabidopsis Book 9, e0148
| Phytochrome signaling mechanisms.Crossref | GoogleScholarGoogle Scholar | 22303272PubMed |

Li Z-G, Ding X-J, Du P-F (2013) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. Journal of Plant Physiology 170, 741–747.
| Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline.Crossref | GoogleScholarGoogle Scholar | 23523123PubMed |

Lin C (2002) Blue light receptors and signal transduction. The Plant Cell 14, S207–S225.
| Blue light receptors and signal transduction.Crossref | GoogleScholarGoogle Scholar | 12045278PubMed |

Liu Z-Q, Yan L, Wu Z, Mei C, Lu K, Yu Y-T, Liang S, Zhang X-F, Wang X-F, Zhang D-P (2012) Cooperation of three WRKY-domain transcription factors WRKY18, WRKY40, and WRKY60 in repressing two ABA-responsive genes ABI4 and ABI5 in Arabidopsis. Journal of Experimental Botany 63, 6371–6392.
| Cooperation of three WRKY-domain transcription factors WRKY18, WRKY40, and WRKY60 in repressing two ABA-responsive genes ABI4 and ABI5 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 23095997PubMed |

Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants – from the field to the test tube and back. Plant Biology 9, 582–588.
| Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants – from the field to the test tube and back.Crossref | GoogleScholarGoogle Scholar | 17853358PubMed |

Park E, Kim J, Lee Y, Shin J, Oh E, Chung WI, Liu J, Choi G (2004) Degradation of phytochrome interacting factor 3 in phytochrome-mediated light signaling. Plant & Cell Physiology 45, 968–975.
| Degradation of phytochrome interacting factor 3 in phytochrome-mediated light signaling.Crossref | GoogleScholarGoogle Scholar |

Patil GG, Oi R, Gissinger A, Moe R (2001) Plant morphology is affected by light quality selective plastic films and alternating day and night temperature. Gartenbauwissenschaft 66, 53–60.

Pham VN, Kathare PK, Huq E (2018) Phytochromes and phytochrome interacting factors. Plant Physiology 176, 1025–1038.
| Phytochromes and phytochrome interacting factors.Crossref | GoogleScholarGoogle Scholar | 29138351PubMed |

Qiao Z, Jing T, Liu Z, Zhang L, Jin Z, Liu D, Pei Y (2015) H2S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis. Plant and Soil 393, 137–146.
| H2S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Riemenschneider A, Wegele R, Schmidt A, Papenbrock J (2005) Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS Journal 272, 1291–1304.
| Isolation and characterization of a D-cysteine desulfhydrase protein from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 15720402PubMed |

Sharrock RA (2002) Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiology 130, 442–456.
| Patterns of expression and normalized levels of the five Arabidopsis phytochromes.Crossref | GoogleScholarGoogle Scholar | 12226523PubMed |

Shen H, Zhu L, Castillon A, Majee M, Downie B, Huq E (2008) Light-induced phosphorylation and degradation of the negative regulator PHYTOCHROME-INTERACTING FACTOR1 from Arabidopsis depend upon its direct physical interactions with photoactivated phytochromes. The Plant Cell 20, 1586–1602.
| Light-induced phosphorylation and degradation of the negative regulator PHYTOCHROME-INTERACTING FACTOR1 from Arabidopsis depend upon its direct physical interactions with photoactivated phytochromes.Crossref | GoogleScholarGoogle Scholar | 18539749PubMed |

Shi H, Ye T, Chan Z (2013) Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiology and Biochemistry 71, 226–234.
| Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.).Crossref | GoogleScholarGoogle Scholar | 23974354PubMed |

Shor E, Paik I, Kangisser S, Green R, Huq E (2017) PHYTOCHROME INTERACTING FACTORS mediate metabolic control of the circadian system in Arabidopsis. New Phytologist 215, 217–228.
| PHYTOCHROME INTERACTING FACTORS mediate metabolic control of the circadian system in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 28440582PubMed |

Tian B, Zhang Y, Jin Z, Liu Z, Pei Y (2017) Role of hydrogen sulfide in the methyl jasmonate response to cadmium stress in foxtail millet. Frontiers in Bioscience 22, 530–538.
| Role of hydrogen sulfide in the methyl jasmonate response to cadmium stress in foxtail millet.Crossref | GoogleScholarGoogle Scholar |

Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiological Reviews 92, 791–896.
| Physiological implications of hydrogen sulfide: a whiff exploration that blossomed.Crossref | GoogleScholarGoogle Scholar | 22535897PubMed |

Wilson LG, Bressan RA, Filner P (1978) Light-dependent emission of hydrogen sulfide from plants. Plant Physiology 61, 184–189.
| Light-dependent emission of hydrogen sulfide from plants.Crossref | GoogleScholarGoogle Scholar | 16660257PubMed |

Xu X, Chi W, Sun X, Feng P, Guo H, Li J, Lin R, Lu C, Wang H, Leister D, Zhang L (2016) Convergence of light and chloroplast signals for de-etiolation through ABI4–HY5 and COP1. Nature Plants 2, 16066
| Convergence of light and chloroplast signals for de-etiolation through ABI4–HY5 and COP1.Crossref | GoogleScholarGoogle Scholar | 27255835PubMed |

Zhang H, Hu L, Hu K, He Y, Wang S, Luo J (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. Journal of Integrative Plant Biology 50, 1518–1529.
| Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress.Crossref | GoogleScholarGoogle Scholar | 19093970PubMed |

Zhang H, Hu S, Zhang Z, Hu L, Jiang C (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biology and Technology 60, 251–257.
| Hydrogen sulfide acts as a regulator of flower senescence in plants.Crossref | GoogleScholarGoogle Scholar |

Zhang G, Liu X, Quan Z, Cheng S, Xu X, Pan S, Xie M, Zeng P, Yue Z, Wang W, et al. (2012) Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nature Biotechnology 30, 549–554.
| Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential.Crossref | GoogleScholarGoogle Scholar | 22580950PubMed |

Zhang L, Pei Y, Wang H, Jin Z, Liu Z, Qiao Z, Fang H, Zhang Y (2015) Hydrogen sulfide alleviates cadmium-induced cell death through restraining ROS accumulation in roots of Brassica rapa L. ssp. pekinensis. Oxidative Medicine and Cellular Longevity 2015, 804603

Zhang Q, Chen K, Zhao Y (2018) Effects of different LED light sources on photosynthetic characteristics, physiological quality and protective enzyme system of watermelon seedlings. Journal of Shanxi Agricultural Sciences 46, 1615–1617.