Diversity of a cytokinin dehydrogenase gene in wild and cultivated barley
Autoři:
Beata I. Czajkowska aff001; Conor M. Finlay aff002; Glynis Jones aff003; Terence A. Brown aff001
Působiště autorů:
Department of Earth and Environmental Sciences, Manchester Institute of Biotechnology, University of Manchester, Manchester, England, United Kingdom
aff001; Lydia Becker Institute of Immunology and Inflammation, School of Biological Sciences, University of Manchester, Manchester, England, United Kingdom
aff002; Department of Archaeology, University of Sheffield, Northgate House, West Street, Sheffield, England, United Kingdom
aff003
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225899
Souhrn
The cytokinin dehydrogenase gene HvCKX2.1 is the regulatory target for the most abundant heterochromatic small RNAs in drought-stressed barley caryopses. We investigated the diversity of HvCKX2.1 in 228 barley landraces and 216 wild accessions and identified 14 haplotypes, five of these with ten or more members, coding for four different protein variants. The third largest haplotype was abundant in wild accessions (51 members), but absent from the landrace collection. Protein structure predictions indicated that the amino acid substitution specific to haplotype 3 could result in a change in the functional properties of the HvCKX2.1 protein. Haplotypes 1–3 have overlapping geographical distributions in the wild population, but the average rainfall amounts at the collection sites for haplotype 3 plants are significantly higher during November to February compared to the equivalent data for plants of haplotypes 1 and 2. We argue that the likelihood that haplotype 3 plants were excluded from landraces by sampling bias that occurred when the first wild barley plants were taken into cultivation is low, and that it is reasonable to suggest that plants with haplotype 3 are absent from the crop because these plants were less suited to the artificial conditions associated with cultivation. Although the cytokinin signalling pathway influences many aspects of plant development, the identified role of HvCKX2.1 in the drought response raises the possibility that the particular aspect of cultivation that mitigated against haplotype 3 relates in some way to water utilization. Our results therefore highlight the possibility that water utilization properties should be looked on as a possible component of the suite of physiological adaptations accompanying the domestication and subsequent evolution of cultivated barley.
Klíčová slova:
Haplotypes – Maize – Sequence alignment – Protein structure – Protein structure comparison – Protein structure prediction – Barley – Cytokinins
Zdroje
1. Abbo S, Gopher A, Rubin B, Lev-Yadun S. On the origin of Near Eastern founder crops and the ‘dump-heap hypothesis’. Genet Resour Crop Evol. 2005; 52: 491–495.
2. Zeder MA. Central questions in the domestication of plants and animals. Evol Anthropol. 2006; 15: 105–117.
3. Zeder MA. Domestication and early agriculture in the Mediterranean Basin: origins, diffusion, and impact. Proc Natl Acad Sci USA. 2008; 105: 11597–11604. doi: 10.1073/pnas.0801317105 18697943
4. Brown TA, Jones MK, Powell W, Allaby RG. The complex origins of domesticated crops in the Fertile Crescent. Trends Ecol Evol. 2009; 24: 103–109. doi: 10.1016/j.tree.2008.09.008 19100651
5. Fuller DQ. An emerging paradigm shift in the origins of agriculture. Gen Anthropol. 2010; 17(1): 8–12.
6. Abbo S, Gopher A. Near Eastern plant domestication: a history of thought. Trends Plant Sci. 2017; 22: 491–511. doi: 10.1016/j.tplants.2017.03.010 28434795
7. Zohary D, Hopf M, Weiss E. Domestication of Plants in the Old World, 4th edn. Oxford: Oxford University Press; 2012.
8. Hammer K. Das Domestikationssyndrom. Kulturpflanze. 1984; 32: 11–34.
9. Fuller DQ. Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World. Annals Bot. 2007; 100: 903–924.
10. Gepts P. Crop domestication as a long-term selection experiment. Plant Breed Rev. 2004; 24: 1–44.
11. Abbo S, Lev-Yadun S, Gopher A. Agricultural origins: centers and non-centers; a Near Eastern reappraisal. Crit Rev Plant Sci. 2010; 29: 317–328.
12. Riehl S, Pustovoytov KE, Weippert H, Klett S, Hole F. Drought stress variability in ancient Near Eastern agricultural systems evidenced by δ13C in barley grain. Proc Natl Acad Sci USA. 2014; 111: 12348–12353. doi: 10.1073/pnas.1409516111 25114225
13. Mithen S. The domestication of water: water management in the ancient world and its prehistoric origins in the Jordan Valley. Phil Trans R Soc A. 2010; 368: 5249–5274. doi: 10.1098/rsta.2010.0191 20956370
14. Wallace MP, Jones G, Charles M, Fraser R, Heaton THE, Bogaard A. Stable carbon isotope evidence for Neolithic and Bronze Age crop water management in the Eastern Mediterranean and Southwest Asia. PLoS ONE. 2015; 10(6): e0127085. doi: 10.1371/journal.pone.0127085 26061494
15. Farquhar G, Richards R. Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aus J Plant Physiol. 1984. 11: 539–552.
16. Araus J, Buxó R. Changes in carbon isotope discrimination in grain cereals from the north-western Mediterranean Basin during the past seven millennia. Aus J Plant Physiol. 1993; 20: 117–128.
17. Araus J, Febrero A, Buxó R, Rodríguez-Ariza M, Molina F, Camalich MD, et al. Identification of ancient irrigation practices based on the carbon isotope discrimination of plant seeds: a case study from the South-East Iberian Peninsula. J Archaeol Sci. 1997; 24: 729–740.
18. Araus J, Febrero A, Catala M, Molist M, Voltas J, Romagosa I, et al. Crop water availability in early agriculture: evidence from carbon isotope discrimination of seeds from a tenth millennium BP site on the Euphrates. Glob Change Biol. 1999; 5: 201–212.
19. Ferrio JP, Araus JL, Buxó R, Voltas J, Bort J. Water management practices and climate in ancient agriculture: inferences from the stable isotope composition of archaeobotanical remains. Veget Hist Archaeobot. 2005; 14: 510–517.
20. Riehl S, Bryson R, Pustovoytov K. Changing growing conditions for crops during the Near Eastern Bronze Age (3000–1200 BC): the stable carbon isotope evidence. J Archaeol Sci. 2008; 35: 1011–1022.
21. Jones G, Charles M, Colledge S, Halstead, P. Towards the archaeobotanical recognition of winter cereal irrigation: an investigation of modern weed ecology in northern Spain. In Kroll H, Pasternak R, editors. Res Archaeobotanicae–International Workgroup for Palaeoethnobotany (Proceedings of the 9th Symposium, Kiel 1992). Kiel: Oetker-Voges-Verlag; 1995. pp. 49–68.
22. Jones G, Charles M, Bogaard A, Hodgson J, Palmer C. The functional ecology of present-day arable weed floras and its applicability for the identification of past crop husbandry. Veget Hist Archaeobot. 2005; 14: 493–504.
23. Jones G, Charles M, Bogaard A, Hodgson J. Crops and weeds: the role of weed functional ecology in the identification of crop husbandry methods. J Archaeol Sci. 2010; 37: 70–77.
24. Charles M, Jones G. FIBS in archaeobotany: functional interpretation of weed floras in relation to husbandry practices. J Archaeol Sci. 1997; 24: 1151–1161.
25. Charles M, Hoppé C. The effects of irrigation on the weed floras of winter cereal crops in Wadi Ibn Hamad (Southern Jordan). Levant. 2003; 35: 213–230.
26. Charles M, Hoppé C, Jones G, Bogaard A, Hodgson J. Using weed functional attributes for the identification of irrigation regimes in Jordan. J Archaeol Sci. 2003; 30: 1429–1441.
27. Honsdorf N, March TJ, Berger B, Tester M, Pillen K. High-throughput phenotyping to detect drought tolerance QTL in wild barley introgression lines. PLoS ONE. 2014; 9(5): e97047. doi: 10.1371/journal.pone.0097047 24823485
28. Hu H, Xiong L. Genetic engineering and breeding of drought-resistance crops. Ann Rev Plant Biol. 2014; 65: 715–741.
29. Nuccio ML, Paul M, Bate NJ, Cohn J, Cutler SR. Where are the drought tolerant crops? An assessment of more than two decades of plant biotechnology effort in crop improvement. Plant Sci. 2018; 273: 110–119. doi: 10.1016/j.plantsci.2018.01.020 29907303
30. Wilkinson S, Kudoyarova GR, Veselov DS, Arkhipova TN, Davies WJ. Plant hormone interactions: innovative targets for crop breeding and management. J Exp Bot. 2012; 63: 3499–3509. doi: 10.1093/jxb/ers148 22641615
31. Wilkinson S, Davies WJ. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ. 2010; 33: 510–525. doi: 10.1111/j.1365-3040.2009.02052.x 19843256
32. Basu S, Ramegowda V, Kumar A, Pereira A. Plant adaptation to drought stress. F1000 Res. 2016; 5: 1554.
33. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. Abscisic acid: emergence of a core signaling network. Ann Rev Plant Biol. 2010; 61: 651–679.
34. Budak H, Akpinar BA. Plant miRNAs: biogenesis, organization and origins. Funct Integr Genet. 2015; 15: 523–531.
35. Matzke MA, Kanno T, Matzke AJ. RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Ann Rev Plant Biol. 2015; 66: 243–267.
36. Ferdous J, Hussain SS, Shi BJ. Role of microRNAs in plant drought tolerance. Plant Biotechnol J. 2015; 13: 293–305. doi: 10.1111/pbi.12318 25583362
37. Surdonja K, Eggert K, Hajirezaei M-R, Harshavardhan VT, Seiler C, von Wirén N, et al. Increase of DNA methylation at the HvCKX2.1 promoter by terminal drought stress in barley. Epigenomes. 2017; 1: 9.
38. Galuszka P, Frébort I, Šebela M, Sauer P, Jacobsen S, Peč P. Cytokinin oxidase or dehydrogenase? Mechanism of cytokinin degradation in cereals. Eur J Biochem. 2001; 268: 450–461. doi: 10.1046/j.1432-1033.2001.01910.x 11168382
39. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012; 28: 1647–1649. doi: 10.1093/bioinformatics/bts199 22543367
40. Bandelt H-J, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999; 16: 37–48. doi: 10.1093/oxfordjournals.molbev.a026036 10331250
41. Leigh JW, Bryant D. PopART: Full-feature software for haplotype network construction. Methods Ecol Evol. 2015; 6: 1110–1116.
42. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011; 7: 539. doi: 10.1038/msb.2011.75 21988835
43. Rice P, Longden I, Bleasby A. EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 2000; 16: 276–277. doi: 10.1016/s0168-9525(00)02024-2 10827456
44. Fick SE, Hijmans RJ. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol. 2017; 37: 4302–4315.
45. Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron. 2001; 4: 9–18.
46. R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2017. Available from: https://www.R-project.org/
47. Malito E, Coda A, Bilyeu KD, Fraaije MW, Mattevi A. Structures of Michaelis and product complexes of plant cytokinin dehydrogenase: implications for flavoenzyme catalysis. J Mol Biol. 2004; 341: 1237–1249. doi: 10.1016/j.jmb.2004.06.083 15321719
48. Kopečný D, Končitíková R, Popelka H, Briozzo P, Vigouroux A, Kopečná M, et al. Kinetic and structural investigation of the cytokinin oxidase/dehydrogenase active site. FEBS J. 2016; 283: 361–377. doi: 10.1111/febs.13581 26519657
49. Poets AM, Fang Z, Clegg MT, Morrell PL. Barley landraces are characterized by geographically heterogeneous genomic origins. Genome Biol. 2015; 16: 173. doi: 10.1186/s13059-015-0712-3 26293830
50. Pankin A, Altmüller J, Becker C., von Korff M. Targeted resequencing reveals genomic signatures of barley domestication. New Phytol. 2018; 218: 1247–1259. doi: 10.1111/nph.15077 29528492
51. Keiber JJ, Schaller GE. Cytokinin signalling in plant development. Development 2018; 145: dev149344. doi: 10.1242/dev.149344 29487105
52. Cunniff J, Wilkinson S, Charles M, Jones G, Rees M, Osborne CP. Functional traits differ between cereal crop progenitors and other wild grasses gathered during the Neolithic in southwest Asia. PLoS ONE. 2014; 9(1): e87586. doi: 10.1371/journal.pone.0087586 24489941
53. Preece C, Livarda A, Christin P-A, Wallace M, Martin G, Charles M, et al. How did domestication of Fertile Crescent grain crops increase their yields? Funct Ecol. 2017; 31: 387–397. doi: 10.1111/1365-2435.12760 28286354
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts