Functional characterization of Arabidopsis hydroxynitrile lyase in response to abiotic stress and the regulation of flowering time.


Journal

Molecular biology reports
ISSN: 1573-4978
Titre abrégé: Mol Biol Rep
Pays: Netherlands
ID NLM: 0403234

Informations de publication

Date de publication:
28 Sep 2024
Historique:
received: 07 06 2024
accepted: 19 09 2024
medline: 29 9 2024
pubmed: 28 9 2024
entrez: 28 9 2024
Statut: epublish

Résumé

Hydroxynitrile lyases (HNLs) are a class of hydrolytic enzymes from a wide range of sources, which play crucial roles in the catalysis of the reversible conversion of carbonyl compounds derived from cyanide and free cyanide in cyanogenic plant species. HNLs were also discovered in non-cyanogenic plants, such as Arabidopsis thaliana, and their roles remain unclear even during plant growth and reproduction. The pattern of expression of the HNL in A. thaliana (AtHNL) in different tissues, as well as under abiotic stresses and hormone treatments, was examined by real-time quantitative reverse transcription PCR (qRT-PCR) and an AtHNL promoter-driven histochemical β-glucuronidase (GUS) assay. AtHNL is highly expressed in flowers and siliques, and the expression of AtHNL was dramatically affected by abiotic stresses and hormone treatments. The overexpression of AtHNL resulted in transgenic A. thaliana seedlings that were more tolerance to mannitol and salinity. Moreover, transgenic lines of A. thaliana that overexpressed this gene were less sensitive to abscisic acid (ABA). Altered expression of ABA/stress responsive genes was also observed in hnl mutant and AtHNL-overexpressing plants, suggesting AtHNL may play functional roles on regulating Arabidopsis resistance to ABA and abiotic stresses by affecting ABA/stress responsive gene expression. In addition, the overexpression of AtHNL resulted in earlier flowering, whereas the AtHNL mutant flowered later than the wild type (WT) plants. The expression of the floral stimulators CONSTANS (CO), SUPPRESSOR OF OVER EXPRESSION OF CO 1 (SOC1) and FLOWERING LOCUS T (FT) was upregulated in plants that overexpressed AtHNL when compared with the WT plants. In contrast, expression of the floral repressor FLOWERING LOCUS C (FLC) was upregulated in AtHNL mutants and downregulated in plants that overexpressed AtHNL compared to the WT plants. This study revealed that AtHNL can be induced under abiotic stresses and ABA treatment, and genetic analysis showed that AtHNL could also act as a positive regulator of abiotic stress and ABA tolerance, as well as flowering time.

Sections du résumé

BACKGROUND BACKGROUND
Hydroxynitrile lyases (HNLs) are a class of hydrolytic enzymes from a wide range of sources, which play crucial roles in the catalysis of the reversible conversion of carbonyl compounds derived from cyanide and free cyanide in cyanogenic plant species. HNLs were also discovered in non-cyanogenic plants, such as Arabidopsis thaliana, and their roles remain unclear even during plant growth and reproduction.
METHODS AND RESULTS RESULTS
The pattern of expression of the HNL in A. thaliana (AtHNL) in different tissues, as well as under abiotic stresses and hormone treatments, was examined by real-time quantitative reverse transcription PCR (qRT-PCR) and an AtHNL promoter-driven histochemical β-glucuronidase (GUS) assay. AtHNL is highly expressed in flowers and siliques, and the expression of AtHNL was dramatically affected by abiotic stresses and hormone treatments. The overexpression of AtHNL resulted in transgenic A. thaliana seedlings that were more tolerance to mannitol and salinity. Moreover, transgenic lines of A. thaliana that overexpressed this gene were less sensitive to abscisic acid (ABA). Altered expression of ABA/stress responsive genes was also observed in hnl mutant and AtHNL-overexpressing plants, suggesting AtHNL may play functional roles on regulating Arabidopsis resistance to ABA and abiotic stresses by affecting ABA/stress responsive gene expression. In addition, the overexpression of AtHNL resulted in earlier flowering, whereas the AtHNL mutant flowered later than the wild type (WT) plants. The expression of the floral stimulators CONSTANS (CO), SUPPRESSOR OF OVER EXPRESSION OF CO 1 (SOC1) and FLOWERING LOCUS T (FT) was upregulated in plants that overexpressed AtHNL when compared with the WT plants. In contrast, expression of the floral repressor FLOWERING LOCUS C (FLC) was upregulated in AtHNL mutants and downregulated in plants that overexpressed AtHNL compared to the WT plants.
CONCLUSION CONCLUSIONS
This study revealed that AtHNL can be induced under abiotic stresses and ABA treatment, and genetic analysis showed that AtHNL could also act as a positive regulator of abiotic stress and ABA tolerance, as well as flowering time.

Identifiants

pubmed: 39340719
doi: 10.1007/s11033-024-09957-w
pii: 10.1007/s11033-024-09957-w
doi:

Substances chimiques

Aldehyde-Lyases EC 4.1.2.-
Abscisic Acid 72S9A8J5GW
mandelonitrile lyase EC 4.1.2.10
Arabidopsis Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1025

Subventions

Organisme : the "333 project" of Jiangsu Province
ID : BRA2015432
Organisme : the National Natural Science Foundation of China
ID : 31301798

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Zagrobelny M, Bak S, Møller BL (2008) Cyanogenesis in plants and arthropods. Phytochemistry 69:1457–1468. https://doi.org/10.1016/j.phytochem.2008.02.019
doi: 10.1016/j.phytochem.2008.02.019 pubmed: 18353406
Jangir N, Padhi SK (2019) Immobilized Baliospermum montanum hydroxynitrile lyase catalyzed synthesis of chiral cyanohydrins. Bioorg Chem 84:32–40. https://doi.org/10.1016/j.bioorg.2018.11.017
doi: 10.1016/j.bioorg.2018.11.017 pubmed: 30481644
Guan XE, Miao RP, Hua X et al (2023) Biocatalytic enantioselective synthesis of chiral β-hydroxy nitriles using cyanohydrins as cyano sources. ACS Catal 13:13597–13606. https://doi.org/10.1021/acscatal.3c03173
doi: 10.1021/acscatal.3c03173
Vetter J (2000) Plant cyanogenic glycosides. Toxicon 38:11–36. https://doi.org/10.1016/S0041-0101(99)00128-2
doi: 10.1016/S0041-0101(99)00128-2 pubmed: 10669009
Lieberei R, Selmar D, Biehl B (1985) Metabolization of cyanogenic glucosides in Hevea brasiliensis. Plant Syst Evol 150:49–63. https://doi.org/10.1007/BF00985567
doi: 10.1007/BF00985567
Gleadow RM, Woodrow IE (2002) Mini-review: constraints on effectiveness of cyanogenic glycosides in herbivore defense. J Chem Ecol 28:1301–1313. https://doi.org/10.1023/A:1016298100201
doi: 10.1023/A:1016298100201 pubmed: 12199497
Zagrobelny M, Bak S, Rasmussen AV et al (2004) Cyanogenic glucosides and plant–insect interactions. Phytochemistry 65:293–306. https://doi.org/10.1016/j.phytochem.2003.10.016
doi: 10.1016/j.phytochem.2003.10.016 pubmed: 14751300
Grossmann K (1996) A role for cyanide, derived from ethylene biosynthesis, in the development of stress symptoms. Physiol Plant 97:772–775. https://doi.org/10.1111/j.1399-3054.1996.tb00543.x
doi: 10.1111/j.1399-3054.1996.tb00543.x
Bogatek R, Côme D, Corbineau F et al (1999) Sugar metabolism as related to the cyanide–mediated elimination of dormancy in apple embryos. Plant Physiol Biochem 37:577–585. https://doi.org/10.1016/S0981-9428(00)80110-2
Siegień I, Bogatek R (2006) Cyanide action in plants–from toxic to regulatory. Acta Physiol Plant 28:483–497. https://doi.org/10.1007/BF02706632
doi: 10.1007/BF02706632
Peterson CJ, Tsao R, Eggler AL et al (2000) Insecticidal activity of cyanohydrin and monoterpenoid compounds. Molecules 5:648–654. https://doi.org/10.3390/50400648
Andexer J, Guterl JK, Pohl M et al (2006) A high-throughput screening assay for hydroxynitrile lyase activity. Chem Commun 40:4201–4203. https://doi.org/10.1039/B607863J
Dadashipour M, Asano Y (2011) Hydroxynitrile lyase: insights into biochemistry, discover, and engineering. ACS Catal 1:1121–1149. https://doi.org/10.1021/cs200325q
Zheng D, Nakabayashi M, Asano Y (2022) Structural characterization of Linum usitatissimum hydroxynitrile lyase: a new cyanohydrin decomposition mechanism involving a cyano-zinc complex. J Biol Chem 298:101650. https://doi.org/10.1016/j.jbc.2022.101650
doi: 10.1016/j.jbc.2022.101650 pubmed: 35101448 pmcid: 8892092
Andexer J, von Langermann J, Mell A et al (2007) An R-selective hydroxynitrile lyase from Arabidopsis thaliana with an α/β-hydrolase fold. Angew Chem Int Ed 46:8679–8681. https://doi.org/10.1002/anie.200701455
Fuhshuku KI, Asano Y (2011) Synthesis of (R)-β-nitro alcohols catalyzed by R-selective hydroxynitrile lyase from Arabidopsis thaliana in the aqueous–organic biphasic system. J Biotechnol 153:153–159. https://doi.org/10.1016/j.jbiotec.2011.03.011
Arnaiz A, Santamaria ME, Rosa-Diaz I et al (2022) Hydroxynitrile lyase defends Arabidopsis against Tetranychus urticae. Plant Physiol 189:2244–2258. https://doi.org/10.1093/plphys/kiac170
doi: 10.1093/plphys/kiac170 pubmed: 35474139 pmcid: 9342993
Simpson SD, Nakashima K, Narusaka Y et al (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259–270. https://doi.org/10.1046/j.1365-313X.2003.01624.x
Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037. https://doi.org/10.1007/s00018-011-0673-y
doi: 10.1007/s00018-011-0673-y pubmed: 21611891 pmcid: 11115107
Quiroz S, Yustis JC, Chávez-Hernández EC et al (2021) Beyond the genetic pathways, flowering regulation complexity in Arabidopsis thaliana. Int J Mol Sci 22:5716. https://doi.org/10.3390/ijms22115716
doi: 10.3390/ijms22115716 pubmed: 34071961 pmcid: 8198774
Helliwell CA, Wood CC, Robertson M et al (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J 46:183–192. https://doi.org/10.1111/j.1365-313X.2006.02686.x
Corbesier L, Vincent C, Jang S et al (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033. https://doi.org/10.1126/science.1141752
Searle I, He YH, Turck F et al (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev 20:898–912. https://doi.org/10.1101/gad.373506
He Y (2009) Control of the transition to flowering by chromatin modifications. Mol Plant 2:554–564. https://doi.org/10.1093/mp/ssp005
doi: 10.1093/mp/ssp005 pubmed: 19825638
Liu F, Marquardt S, Lister C et al (2012) Targeted 3’ processing of antisense transcripts triggers ArabidopsisFLC chromatin silencing. Science 327:94–97. https://doi.org/10.1126/science.1180278
Michaels SD (2009) Flowering time regulation produces much fruit. Curr Opin Plant Biol 12:75–80. https://doi.org/10.1016/j.pbi.2008.09.005
doi: 10.1016/j.pbi.2008.09.005 pubmed: 18938104
He Y (2012) Chromatin regulation of flowering. Trends Plant Sci 17:556–562. https://doi.org/10.1016/j.tplants.2012.05.001
Wang P, Yu S, Han X et al (2020) Identification, molecular characterization and expression of JAZ genes in Lycoris aurea. PLoS ONE 15:e0230177. https://doi.org/10.1371/journal.pone.0230177
doi: 10.1371/journal.pone.0230177 pubmed: 32182273 pmcid: 7077819
Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136. https://doi.org/10.1111/j.1365-313X.2007.03212.x
Sun B, Wang P, Wang R et al (2018) Molecular cloning and characterization of a meta/para-O-methyltransferase from Lycoris aurea. Int J Mol Sci 19:1911. https://doi.org/10.3390/ijms19071911
doi: 10.3390/ijms19071911 pubmed: 29966257 pmcid: 6073595
Wu FH, Shen SC, Lee LY et al (2009) Tape-Arabidopsis Sandwich—a simpler Arabidopsis protoplast isolation method. Plant Methods 5:16. https://doi.org/10.1186/1746-4811-5-16
Nahrstedt A (1985) Cyanogenic compounds as protecting agents for organisms. Plant Syst Evol 150:35–47. https://doi.org/10.1007/BF00985566
doi: 10.1007/BF00985566
García I, Arenas-Alfonseca L, Moreno I et al (2019) HCN regulates cellular processes through posttranslational modification of proteins by S-cyanylation. Plant Physiol 179:107–123. https://doi.org/10.1104/pp.18.01083
Gotor C, García I, Aroca Á et al (2019) Signaling by hydrogen sulfide and cyanide through post-translational modification. J Exp Bot 70:4251–4265. https://doi.org/10.1093/jxb/erz225
Gniazdowska A, Krasuska U, Bogatek R (2010) Dormancy removal in apple embryos by nitric oxide or cyanide involves modifications in ethylene biosynthetic pathway. Planta 232:1397–1407. https://doi.org/10.1007/s00425-010-1262-2
doi: 10.1007/s00425-010-1262-2 pubmed: 20830596
Xu F, Zhang DW, Zhu F et al (2012) A novel role for cyanide in the control of cucumber (Cucumis sativus L.) seedlings response to environmental stress. Plant Cell Environ 35:1983–1997. https://doi.org/10.1111/j.1365-3040.2012.02531.x
doi: 10.1111/j.1365-3040.2012.02531.x pubmed: 22554042
Glawischnig E (2007) Camalexin. Phytochemistry 68:401–406. https://doi.org/10.1016/j.phytochem.2006.12.005
Rajniak J, Barco B, Clay NK et al (2015) A new cyanogenic metabolite in Arabidopsis required for inducible pathogen defense. Nature 525:376–379. https://doi.org/10.1038/nature14907
doi: 10.1038/nature14907 pubmed: 26352477 pmcid: 4629851
Arnaiz A, Martinez M, Gonzalez-Melendi P et al (2019) Plant defenses against pests driven by a bidirectional promoter. Front Plant Sci 10:930. https://doi.org/10.3389/fpls.2019.00930
doi: 10.3389/fpls.2019.00930 pubmed: 31379907 pmcid: 6652247
Pandey GK, Grant JJ, Cheong YH et al (2005) ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis. Plant Physiol 139:1185–1193. https://doi.org/10.1104/pp.105.066324
doi: 10.1104/pp.105.066324 pubmed: 16227468 pmcid: 1283757
Xiang L, Liu C, Luo J et al (2018) A tuber mustard AP2/ERF transcription factor gene, BjABR1, functioning in abscisic acid and abiotic stress responses, and evolutionary trajectory of the ABR1 homologous genes in Brassica species. PeerJ 6:e6071. https://doi.org/10.7717/peerj.6071
doi: 10.7717/peerj.6071 pubmed: 30581669 pmcid: 6294115
Liu W, Thapa P, Park SW (2023) RD29A and RD29B rearrange genetic and epigenetic markers in priming systemic defense responses against drought and salinity. Plant Sci 337:111895. https://doi.org/10.1016/j.plantsci.2023.111895
Chakraborty S, Roychoudhury A (2022) Functional regulation of responsive to abscisic acid (Rab) genes from representative plant species and their stress response. Plant Physiol Rep 27:653–664. https://doi.org/10.1007/s40502-022-00686-5
doi: 10.1007/s40502-022-00686-5
Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2 C involved in abscisic acid signal transduction. Plant Cell 9:759–771. https://doi.org/10.1105/tpc.9.5.759
doi: 10.1105/tpc.9.5.759 pubmed: 9165752 pmcid: 156954
Saez A, Apostolova N, Gonzalez-Guzman M et al (2004) Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2 C HAB1 reveal its role as a negative regulator of abscisic acid signaling. Plant J 37:354–369. https://doi.org/10.1046/j.1365-313X.2003.01966.x
Skubacz A, Daszkowska-Golec A, Szarejko I (2016) The role and regulation of ABI5 (ABA-Insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Front Plant Sci 7:1884. https://doi.org/10.3389/fpls.2016.01884
doi: 10.3389/fpls.2016.01884 pubmed: 28018412 pmcid: 5159420
González-Guzmán M, Apostolova N, Bellés JM et al (2002) The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell 14:1833–1846. https://doi.org/10.1105/tpc.002477
Tanaka O, Cleland CF, Ben-Tal Y (1983) Effect of ferricyanide, ferrocyanide and KCN on growth and flowering in the short-day plant Lemna paucicostata. 6746. Plant Cell Physiol 24:705–711. https://doi.org/10.1093/oxfordjournals.pcp.a076567
doi: 10.1093/oxfordjournals.pcp.a076567
Arenas-Alfonseca L, Gotor C, Romero LC et al (2018) β-Cyanoalanine synthase action in root hair elongation is exerted at early steps of the root hair elongation pathway and is independent of direct cyanide inactivation of NADPH oxidase. Plant Cell Physiol 59:1072–1083. https://doi.org/10.1093/pcp/pcy047
Machingura M, Salomon E, Jez JM (2016) The β-cyanoalanine synthase pathway: beyond cyanide detoxification. Plant Cell Environ 39:2329–2341. https://doi.org/10.1111/pce.12755
Dixit S, Widemann E, Bensoussan N et al (2022) β-Cyanoalanine synthase protects mites against Arabidopsis defenses. Plant Physiol 189:1961–1975. https://doi.org/10.1093/plphys/kiac147
Yang S, Zhang T, Wang Z et al (2022) Nitrilases NIT1/2/3 positively regulate flowering by inhibiting MAF4 expression in Arabidopsis. Front Plant Sci 13:889460. https://doi.org/10.3389/fpls.2022.889460

Auteurs

Lei Xue (L)

Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China.
Jiangsu Key Laboratory for the Research and Utilization of Plant Resources, Nanjing, 210014, China.

Duo Bu (D)

Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China.

Jiangyan Fu (J)

Xuzhou Institute of Agricultural Sciences in Jiangsu Xuhuai District, Xuzhou, 221121, China.

Zhe Zhou (Z)

Department of Basic Medicine, School of Health and Nursing, Wuxi Taihu University, Wuxi, 214000, China.

Meng Gao (M)

Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China.

Ren Wang (R)

Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China. rwang@cnbg.net.
Jiangsu Key Laboratory for the Research and Utilization of Plant Resources, Nanjing, 210014, China. rwang@cnbg.net.

Sheng Xu (S)

Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China. xusheng@cnbg.net.

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