Divergent receptor proteins confer responses to different karrikins in two ephemeral weeds.
Arabidopsis
/ drug effects
Arabidopsis Proteins
Brassica
/ drug effects
Carrier Proteins
/ drug effects
Catalytic Domain
Fires
Furans
/ pharmacology
Gene Expression Regulation, Plant
Germination
/ drug effects
Hydrolases
/ genetics
Magnoliopsida
Plant Proteins
/ drug effects
Plant Weeds
/ drug effects
Pyrans
/ pharmacology
Seedlings
Seeds
/ drug effects
Sequence Analysis, Protein
Transcriptome
Wildfires
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
09 03 2020
09 03 2020
Historique:
received:
18
06
2019
accepted:
12
02
2020
entrez:
11
3
2020
pubmed:
11
3
2020
medline:
3
7
2020
Statut:
epublish
Résumé
Wildfires can encourage the establishment of invasive plants by releasing potent germination stimulants, such as karrikins. Seed germination of Brassica tournefortii, a noxious weed of Mediterranean climates, is strongly stimulated by KAR
Identifiants
pubmed: 32152287
doi: 10.1038/s41467-020-14991-w
pii: 10.1038/s41467-020-14991-w
pmc: PMC7062792
doi:
Substances chimiques
Arabidopsis Proteins
0
Carrier Proteins
0
Furans
0
Plant Proteins
0
Pyrans
0
HTL protein, Arabidopsis
EC 3.-
Hydrolases
EC 3.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1264Références
Early, R. et al. Global threats from invasive alien species in the twenty-first century and national response capacities. Nat. Commun. 7, 12485–12485 (2016).
pubmed: 27549569
pmcid: 4996970
doi: 10.1038/ncomms12485
Flematti, G. R. et al. Karrikin and cyanohydrin smoke signals provide clues to new endogenous plant signaling compounds. Mol. Plant 6, 29–37 (2013).
pubmed: 23180672
doi: 10.1093/mp/sss132
Keeley, J. E. & Pausas, J. G. Evolution of ‘smoke’ induced seed germination in pyroendemic plants. South Afr. J. Bot. 115, 251–255 (2018).
doi: 10.1016/j.sajb.2016.07.012
Flematti, G. R., Ghisalberti, E. L., Dixon, K. W. & Trengove, R. D. Identification of Alkyl substituted 2H-Furo[2,3- c]pyran-2-ones as germination stimulants present in smoke. J. Agric. Food Chem. 57, 9475–9480 (2009).
Hrdlička, J. et al. Quantification of karrikins in smoke water using ultra-high performance liquid chromatography-tandem mass spectrometry. Plant Methods 15, 81 (2019).
pubmed: 31372177
pmcid: 6659305
doi: 10.1186/s13007-019-0467-z
Long, R. L. et al. Detecting karrikinolide responses in seeds of the Poaceae. Aust. J. Bot. 59, 610–620 (2011).
doi: 10.1071/BT11170
Milberg, P. & Lamont, B. B. Fire enhances weed invasion of roadside vegetation in southwestern Australia. Biol. Conserv. 73, 45–49 (1995).
doi: 10.1016/0006-3207(95)90061-6
Flematti, G. R. et al. Preparation of 2H-furo[2,3-c]pyran-2-one derivatives and evaluation of their germination-promoting activity. J. Agric. Food Chem. 55, 2189–2194 (2007).
pubmed: 17316021
doi: 10.1021/jf0633241
Long, R. L. et al. Seeds of Brassicaceae weeds have an inherent or inducible response to the germination stimulant karrikinolide. Ann. Bot. 108, 933–944 (2011).
pubmed: 21821831
pmcid: 3177676
doi: 10.1093/aob/mcr198
Stevens, J., Merritt, D., Flematti, G., Ghisalberti, E. & Dixon, K. Seed germination of agricultural weeds is promoted by the butenolide 3-methyl-2H-furo[2,3-c]pyran-2-one under laboratory and field conditions. Plant Soil 298, 113–124 (2007).
doi: 10.1007/s11104-007-9344-z
Nelson, D. C. et al. Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proc. Natl Acad. Sci. 107, 7095–7100 (2010).
pubmed: 20351290
doi: 10.1073/pnas.0911635107
Kulkarni, M. G., Sparg, S. G., Light, M. E. & Staden, J. V. Stimulation of rice (Oryza sativa L.) seedling vigour by smoke‐water and butenolide. J. Agron. Crop Sci. 192, 395–398 (2006).
doi: 10.1111/j.1439-037X.2006.00213.x
Staden, Jv, Sparg, S. G., Kulkarni, M. G. & Light, M. E. Post-germination effects of the smoke-derived compound 3-methyl-2H-furo[2,3-c]pyran-2-one, and its potential as a preconditioning agent. Field Crop Res. 98, 98–105 (2006).
doi: 10.1016/j.fcr.2005.12.007
Bangle, D. N., Walker, L. R. & Powell, E. A. Seed germination of the invasive plant Brassica tournefortii (Sahara mustard) in the Mojave Desert. West. North Am. Naturalist 68, 334–342 (2008).
doi: 10.3398/1527-0904(2008)68[334:SGOTIP]2.0.CO;2
Brooks, M. L. et al. Effects of invasive alien plants on fire regimes. BioScience 54, 677 (2004).
doi: 10.1641/0006-3568(2004)054[0677:EOIAPO]2.0.CO;2
Sanders R., Minnich R. Brassica tournefortii. In: Invasive Plants of California’s Wildlands (eds. Bossard C. C., Randall J. M., Hoshovsky M. C.). University of California Press (2000).
Schiermeier, Q. Pall hangs over desert’s future as alien weeds fuel wildfires. Nature 435, 724 (2005).
pubmed: 15944662
doi: 10.1038/435724b
Steers R. J. Invasive Plants, Fire succession, and Restoration of Creosote Bush Scrub in Southern California. University of California Riverside (2008).
Sun, X.-D. & Ni, M. HYPOSENSITIVE TO LIGHT, an alpha/beta fold protein, acts downstream of ELONGATED HYPOCOTYL 5 to regulate seedling de-etiolation. Mol. Plant 4, 116–126 (2011).
pubmed: 20864454
doi: 10.1093/mp/ssq055
Waters, M. T. et al. Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139, 1285–1295 (2012).
pubmed: 22357928
doi: 10.1242/dev.074567
Durvasula, A. et al. African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana. Proc. Natl Acad. Sci. 114, 5213–5218 (2017).
pubmed: 28473417
doi: 10.1073/pnas.1616736114
Nelson, D. C. et al. Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiol. 149, 863–873 (2009).
pubmed: 19074625
pmcid: 2633839
doi: 10.1104/pp.108.131516
Flematti, G. R., Ghisalberti, E. L., Dixon, K. W. & Trengove, R. D. A compound from smoke that promotes seed germination. Science 305, 977 (2004).
pubmed: 15247439
doi: 10.1126/science.1099944
Waters, M. T., Gutjahr, C., Bennett, T. & Nelson, D. C. Strigolactone sgnaling and evolution. Annu. Rev. Plant Biol. 68, 291–322 (2017).
pubmed: 28125281
doi: 10.1146/annurev-arplant-042916-040925
Yao, R., Chen, L. & Xie, D. Irreversible strigolactone recognition: a non-canonical mechanism for hormone perception. Curr. Opin. Plant Biol. 45, 155–161 (2018).
pubmed: 30014890
doi: 10.1016/j.pbi.2018.06.007
Scaffidi, A. et al. Exploring the molecular mechanism of karrikins and strigolactones. Bioorg. Medicinal Chem. 22, 3743–3746 (2012).
doi: 10.1016/j.bmcl.2012.04.016
Zwanenburg, B. & Pospíšil, T. Structure and activity of strigolactones: new plant hormones with a rich future. Mol. Plant 6, 38–62 (2013).
pubmed: 23204499
doi: 10.1093/mp/sss141
de Saint Germain, A. et al. An histidine covalent receptor and butenolide complex mediates strigolactone perception. Nat. Chem. Biol. 12, 787–794 (2016).
doi: 10.1038/nchembio.2147
Seto, Y. et al. Strigolactone perception and deactivation by a hydrolase receptor DWARF14. Nat. Commun. 10, 191 (2019).
pubmed: 30643123
pmcid: 6331613
doi: 10.1038/s41467-018-08124-7
Shabek, N. et al. Structural plasticity of D3–D14 ubiquitin ligase in strigolactone signalling. Nature 563, 652–656 (2018).
pubmed: 30464344
pmcid: 6265067
doi: 10.1038/s41586-018-0743-5
Yao, R. et al. DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536, 469–473 (2016).
pubmed: 27479325
doi: 10.1038/nature19073
Marzec, M. & Brewer, P. Binding or hydrolysis? how does the strigolactone receptor work? Trends Plant Sci. 24, 571–574 (2019).
pubmed: 31151745
doi: 10.1016/j.tplants.2019.05.001
Bythell-Douglas, R. et al. Evolution of strigolactone receptors by gradual neo-functionalization of KAI2 paralogues. BMC Biol. 15, 52 (2017).
pubmed: 28662667
pmcid: 5490202
doi: 10.1186/s12915-017-0397-z
Conn, C. E. & Nelson, D. C. Evidence that KARRIKIN-INSENSITIVE2 (KAI2) receptors may perceive an unknown signal that is not karrikin or strigolactone. Front. Plant Sci. 6, 1219 (2015).
pubmed: 26779242
Li, W. et al. The karrikin receptor KAI2 promotes drought resistance in Arabidopsis thaliana. PLoS Genet. 13, e1007076 (2017).
pubmed: 29131815
pmcid: 5703579
doi: 10.1371/journal.pgen.1007076
Sun, Y. K., Flematti, G. R., Smith, S. M. & Waters, M. T. Reporter gene-facilitated detection of compounds in arabidopsis leaf extracts that activate the karrikin signaling pathway. Front. Plant Sci. 7, 1799 (2016).
pubmed: 27994609
pmcid: 5133242
Liu, S. et al. The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat. Commun. 5, 3930 (2014).
pubmed: 24852848
pmcid: 4279128
doi: 10.1038/ncomms4930
Lysak, M. A., Koch, M. A., Pecinka, A. & Schubert, I. Chromosome triplication found across the tribe Brassiceae. Genome Res. 15, 516–525 (2005).
pubmed: 15781573
pmcid: 1074366
doi: 10.1101/gr.3531105
Wang, X. et al. The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43, 1035–1039 (2011).
pubmed: 21873998
doi: 10.1038/ng.919
pmcid: 21873998
Waters, M. T., Scaffidi, A., Flematti, G. & Smith, S. M. Substrate-induced degradation of the α/β-fold hydrolase KARRIKIN INSENSITIVE2 requires a functional catalytic triad but is independent of MAX2. Mol. Plant 8, 814–817 (2015).
pubmed: 25698586
doi: 10.1016/j.molp.2014.12.020
Waters, M. T. et al. A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 functions in arabidopsis development but cannot mediate responses to Karrikins or strigolactones. Plant Cell 27, 1925–1944 (2015).
pubmed: 26175507
pmcid: 4531350
doi: 10.1105/tpc.15.00146
Kagale, S. et al. TMV-gate vectors: gateway compatible tobacco mosaic virus based expression vectors for functional analysis of proteins. Sci. Rep. 2, 874 (2012).
pubmed: 23166857
pmcid: 3500846
doi: 10.1038/srep00874
Yao, J. et al. An allelic series at the KARRIKIN INSENSITIVE 2 locus of Arabidopsis thaliana decouples ligand hydrolysis and receptor degradation from downstream signalling. Plant J. 96, 75–89 (2018).
pubmed: 29982999
doi: 10.1111/tpj.14017
Choi, Y. & Chan, A. P. PROVEAN web server: a tool to predict the functional effect of amino acid substitutions and indels. Bioinformatics 31, 2745–2747 (2015).
pubmed: 25851949
pmcid: 4528627
doi: 10.1093/bioinformatics/btv195
Abe, S. et al. Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc. Natl Acad. Sci. USA 111, 18084–18089 (2014).
pubmed: 25425668
doi: 10.1073/pnas.1410801111
Hamiaux, C. et al. DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr. Biol. 22, 2032–2036 (2012).
pubmed: 22959345
doi: 10.1016/j.cub.2012.08.007
Hamiaux, C. et al. Inhibition of strigolactone receptors by N-phenylanthranilic acid derivatives: structural and functional insights. J. Biol. Chem. 293, 6530–6543 (2018).
pubmed: 29523686
pmcid: 5925799
doi: 10.1074/jbc.RA117.001154
Végh, A. et al. Comprehensive analysis of DWARF14-LIKE2 (DLK2) reveals its functional divergence from strigolactone-related paralogs. Front. Plant Sci. 8, 1641 (2017).
pubmed: 28970845
pmcid: 5609103
doi: 10.3389/fpls.2017.01641
Scaffidi, A. et al. Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol. 165, 1221–1232 (2014).
pubmed: 24808100
pmcid: 4081333
doi: 10.1104/pp.114.240036
Leebens-Mack, J. H. et al. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574, 679–685 (2019).
doi: 10.1038/s41586-019-1693-2
Richardson, D. M., Wilgen, B. W. V. & Mitchell, D. T. Aspects of the reproductive ecology of four australian Hakea species (Proteaceae) in South Africa. Oecologia 71, 345–354 (1987).
pubmed: 28312980
doi: 10.1007/BF00378706
Guo, Y., Zheng, Z., La Clair, J. J., Chory, J. & Noel, J. P. Smoke-derived karrikin perception by the α/β-hydrolase KAI2 from Arabidopsis. Proc. Natl Acad. Sci. USA 110, 8284–8289 (2013).
pubmed: 23613584
doi: 10.1073/pnas.1306265110
Xu, Y. et al. Structural basis of unique ligand specificity of KAI2-like protein from parasitic weed Striga hermonthica. Sci. Rep. 6, 31386 (2016).
pubmed: 27507097
pmcid: 4979206
doi: 10.1038/srep31386
Kagiyama, M. et al. Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells 18, 147–160 (2013).
pubmed: 23301669
doi: 10.1111/gtc.12025
Lee, I. et al. A missense allele of KARRIKIN-INSENSITIVE2 impairs ligand-binding and downstream signaling in Arabidopsis thaliana. J. Exp. Bot. 69, 3609–3623 (2018).
pubmed: 29722815
pmcid: 6022639
doi: 10.1093/jxb/ery164
Yao, J. & Waters, M. T. Perception of karrikins by plants: a continuing enigma. J. Exp. Bot. erz548, https://doi.org/10.1093/jxb/erz1548 (2019).
Conn, C. E. et al. Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349, 540–543 (2015).
pubmed: 26228149
doi: 10.1126/science.aab1140
Toh, S. et al. Structure-function analysis identifies highly sensitive strigolactone receptors in Striga. Science 350, 203–207 (2015).
pubmed: 26450211
doi: 10.1126/science.aac9476
Xu, Y. et al. Structural analysis of HTL and D14 proteins reveals the basis for ligand selectivity in Striga. Nat. Commun. 9, 3947 (2018).
pubmed: 30258184
pmcid: 6158167
doi: 10.1038/s41467-018-06452-2
Bürger, M. et al. Structural basis of Karrikin and non-natural strigolactone perception in Physcomitrella patens. Cell Rep. 26, 855–865 (2019).
pubmed: 30673608
doi: 10.1016/j.celrep.2019.01.003
Shimada, A. et al. Structural basis for gibberellin recognition by its receptor GID1. Nature 456, 520–523 (2008).
pubmed: 19037316
doi: 10.1038/nature07546
Zhang, Y. et al. Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat. Chem. Biol. 10, 1028–1033 (2014).
pubmed: 25344813
doi: 10.1038/nchembio.1660
Challis, R. J., Hepworth, J., Mouchel, C., Waites, R. & Leyser, O. A role for MORE AXILLARY GROWTH1 (MAX1) in evolutionary diversity in strigolactone signaling upstream of MAX2. Plant Physiol. 161, 1885–1902 (2013).
pubmed: 23424248
pmcid: 3613463
doi: 10.1104/pp.112.211383
Brewer, P. B. et al. LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis. Proc. Natl Acad. Sci. 113, 6301–6306 (2016).
pubmed: 27194725
doi: 10.1073/pnas.1601729113
Yoneyama, K. et al. Which are the major players, canonical or non-canonical strigolactones? J. Exp. Bot. 69, 2231–2239 (2018).
pubmed: 29522151
doi: 10.1093/jxb/ery090
Panchy, N., Lehti-Shiu, M. D. & Shiu, S.-H. Evolution of gene duplication in plants. Plant Physiol. 171, 2294–2316 (2016).
pubmed: 27288366
pmcid: 4972278
Wang, L., Waters, M. T. & Smith, S. M. Karrikin-KAI2 signalling provides Arabidopsis seeds with tolerance to abiotic stress and inhibits germination under conditions unfavourable for seedling establishment. New Phytol. 219, 605–618 (2018).
pubmed: 29726620
doi: 10.1111/nph.15192
Goddard-Borger E. D., Ghisalberti E. L., Stick R. V. Synthesis of the germination stimulant 3-methyl-2H-furo[2,3-c]pyran-2-one and analogous compounds from carbohydrates. Eur. J. Org. Chem. 2007, 3925-3934 (2007).
Mangnus, E., Vanvliet, L. A., Vadenput, D. & Zwanenburg, B. Structural modifications of strigol analogs - influence of the B and C rings on the bioactivity of the germination stimulant GR24. J. Agric. Food Chem. 40, 1222–1229 (1992).
doi: 10.1021/jf00019a030
Gorecki, M. J., Long, R. L., Flematti, G. R. & Stevens, J. C. Parental environment changes the dormancy state and karrikinolide response of Brassica tournefortii seeds. Ann. Bot. 109, 1369–1378 (2012).
pubmed: 22492259
pmcid: 3359922
doi: 10.1093/aob/mcs067
Curtis, M. D. & Grossniklaus, U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462–469 (2003).
pubmed: 14555774
pmcid: 523872
doi: 10.1104/pp.103.027979
Flematti, G. R., Scaffidi, A., Dixon, K. W., Smith, S. M. & Ghisalberti, E. L. Production of the seed germination stimulant karrikinolide from combustion of simple carbohydrates. J. Agric. Food Chem. 59, 1195–1198 (2011).
pubmed: 21280622
doi: 10.1021/jf1041728
Liang, C., Liu, X., Yiu, S.-M. & Lim, B. L. De novo assembly and characterization of Camelina sativa transcriptome by paired-end sequencing. BMC Genomics 14, 146 (2013).
pubmed: 23496985
pmcid: 3635884
doi: 10.1186/1471-2164-14-146
Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).
pubmed: 21572440
pmcid: 3571712
doi: 10.1038/nbt.1883
Lefort, V., Longueville, J.-E. & Gascuel, O. SMS: smart model selection in PhyML. Mol. Biol. Evol. 34, 2422–2424 (2017).
pubmed: 28472384
pmcid: 5850602
doi: 10.1093/molbev/msx149
Crooks, G. E., Hon, G., Chandonia, J.-M. & Brenner, S. E. WebLogo: a sequence logo generator. Genome Res 14, 1188–1190 (2004).
pubmed: 15173120
pmcid: 419797
doi: 10.1101/gr.849004
Bordoli, L. et al. Protein structure homology modeling using SWISS-MODEL workspace. Nat. Protoc. 4, 1–13 (2009).
pubmed: 19131951
doi: 10.1038/nprot.2008.197
Dundas, J. et al. CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res. 34, W116–W118 (2006).
pubmed: 16844972
pmcid: 1538779
doi: 10.1093/nar/gkl282
Lopez-Obando, M. et al. Structural modelling and transcriptional responses highlight a clade of PpKAI2-LIKE genes as candidate receptors for strigolactones in Physcomitrella patens. Planta 243, 1441–1453 (2016).
pubmed: 26979323
doi: 10.1007/s00425-016-2481-y