The petunia CHANEL gene is a ZEITLUPE ortholog coordinating growth and scent profiles

Cells

Volumn 8, Issue 4, 2019, Pages

  Terry, Marta I ^a   Pérez Sanz, Fernando ^b   Díaz Galián, M Victoria ^a   de los Cobos, Felipe Pérez ^c   Navarro, Pedro J ^a   Egea Cortines, Marcos ^a   Weiss, Julia ^a  

^a TECHNICAL UNIVERSITY OF CARTAGENA   (Spain)

^b HOSPITAL UNIVERSITARIO VIRGEN DE LA ARRIXACA   (Spain)

^c UNIVERSITY OF MURCIA   (Spain)

Author keywords

Circadian clock; Floral scent; Growth rate; Hairpin RNA; Image analysis; Petal development; Phenomics; ZEITLUPE

Indexed keywords

BENZYL BENZOATE; COMPLEMENTARY DNA; CYCLOPHILIN; ELONGATION FACTOR 1ALPHA; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LIMONENE; MESSENGER RNA; POLYUBIQUITIN; SHORT HAIRPIN RNA;

AMINO ACID SUBSTITUTION; ARTICLE; BIOSYNTHESIS; CIRCADIAN RHYTHM; DNA ISOLATION; DOWN REGULATION; GENE; GENE EXPRESSION; GENE KNOCKDOWN; GENE SEQUENCE; GENE SILENCING; GENETIC ANALYSIS; GENOME; GROWTH RATE; HOUSEKEEPING GENE; IMAGE ANALYSIS; MATHEMATICAL ANALYSIS; NONHUMAN; ORGAN GROWTH; ORGANOGENESIS; PETUNIA; PHOTOSYNTHESIS; PHYLOGENY; PLANT GENE; PLANT GENETICS; PLANT GROWTH; PLANT LEAF; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; TRANSGENIC PLANT;

EID: 85075939203     PISSN: None     EISSN: 20734409     Source Type: Journal    
DOI: 10.3390/cells8040343     Document Type: Article

References (70)

1. Barton, M.K. Twenty years on: The inner workings of the shoot apical meristem, a developmental dynamo. Dev. Biol. 2010, 341, 95-113.
2. Angenent, G.C.; Immink, R.G.H.; Kaufmann, K. The “ABC” of MADS domain protein behaviour and interactions. Semin. Cell Dev. Biol. 2010, 21, 87-93.
3. Egea-Cortines, M.; Saedler, H.; Sommer, H. Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J. 1999, 18, 5370-5379.
4. Honma, T.; Goto, K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 2001, 409, 525-529.
5. Bernardello, G.; Anderson, G.J.; Stuessy, T.F.; Crawford, D.J. A survey of floral traits, breeding systems, floral visitors, and pollination systems of the angiosperms of the Juan Fernandez Islands (Chile). Bot. Rev. 2001, 67, 255-308.
6. Hepworth, J.; Lenhard, M. Regulation of plant lateral-organ growth by modulating cell number and size. Curr. Opin. Plant Biol. 2014, 17, 36-42.
7. Manchado-Rojo, M.; Weiss, J.; Egea-Cortines, M. Validation of Aintegumenta as a gene to modify floral size in ornamental plants. Plant Biotechnol. J. 2014, 12, 1053-1065.
8. Krizek, B.A. Ectopic expression AINTEGUMENTA in Arabidopsis plants results in increased growth of floral organs. Dev. Genet. 1999, 25, 224-236.
9. Kuluev, B.; Avalbaev, A.; Nurgaleeva, E.; Knyazev, A.; Nikonorov, Y.; Chemeris, A. Role of AINTEGUMENTA-like gene NtANTL in the regulation of tobacco organ growth. J. Plant Physiol. 2015, 189, 11-23.
10. Muhlemann, J.K.; Maeda, H.; Chang, C.Y.; Miguel, P.S.; Baxter, I.; Cooper, B.; Perera, M.A.; Nikolau, B.J.; Vitek, O.; Morgan, J.A., et al. Developmental Changes in the Metabolic Network of Snapdragon Flowers. PLoS ONE 2012, 7, e40381.
11. Manchado-Rojo, M.; Delgado-Benarroch, L.; Roca, M.J.; Weiss, J.; Egea-Cortines, M. Quantitative levels of Deficiens and Globosa during late petal development show a complex transcriptional network topology of B function. Plant J. 2012, 72, 294-307.
12. Fenske, M.P.; Imaizumi, T. Circadian Rhythms in Floral Scent Emission. Front. Plant Sci. 2016, 7, 462.
13. Dudareva, N.; Murfitt, L.M.; Mann, C.J.; Gorenstein, N.; Kolosova, N.; Kish, C.M.; Bonham, C.; Wood, K. Developmental regulation of methyl benzoate biosynthesis and emission in snapdragon flowers. Plant Cell 2000, 12, 949-961.
14. Verdonk, J.C.; Ric de Vos, C.H.; Verhoeven, H.A.; Haring, M.A.; van Tunen, A.J.; Schuurink, R.C.; de Vos, C.H.R. Regulation of floral scent production in petunia revealed by targeted metabolomics. Phytochemistry 2003, 62, 997-1008.
15. Hendel-Rahmanim, K.; Masci, T.; Vainstein, A.; Weiss, D. Diurnal regulation of scent emission in rose flowers. Planta 2007, 226, 1491-1499.
16. Ruíz-Ramón, F.; Águila, D.J.; Egea-Cortines, M.; Weiss, J. Optimization of fragrance extraction: Daytime and flower age affect scent emission in simple and double narcissi. Ind. Crops Prod. 2014, 52, 671-678.
17. Yon, F.; Joo, Y.; Cort, L.; Rothe, E.; Baldwin, I.T.; Kim, S.; Kim, S. Silencing Nicotiana attenuata LHY and ZTL alters circadian rhythms in flowers. New Phytol. 2015, 203, 1058-1066.
18. Fenske, M.P.; Hewett Hazelton, K.D.; Hempton, A.K.; Shim, J.S.; Yamamoto, B.M.; Riffell, J.A.; Imaizumi, T. Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia. Proc. Natl. Acad. Sci. USA 2015, 112, 9775-9780.
19. Bombarely, A.; Moser, M.; Amrad, A.; Bao, M.; Bapaume, L.; Barry, C.C.S.; Bliek, M.; Boersma, M.R.M.; Borghi, L.; Bruggmann, R., et al. Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida. Nat. Plants 2016, 2, 1-9.
20. Birney, E.; Clamp, M.; Durbin, R. GeneWise and Genomewise. Genome Res. 2004, 14, 988-995.
21. Larkin, M.A.; Blackshields, G.; Brown, N.P.; Chenna, R.; McGettigan, P.A.; McWilliam, H.; Valentin, F.; Wallace, I.M.; Wilm, A.; Lopez, R., et al. Clustal W and clustal X version 2.0. Bioinformatics 2007, 23, 2947-2948.
22. Paradis, E.; Claude, J.; Strimmer, K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 2004, 20, 289-290.
23. Schliep, K.P. Phangorn: Phylogenetic analysis in R. Bioinformatics 2011, 27, 592-593.
24. Yu, G.; Smith, D.K.; Zhu, H.; Guan, Y.; Lam, T.T.-Y. Ggtree: An r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol. 2017, 8, 28-36.
25. Helliwell, C.; Waterhouse, P. Constructs and methods for high-throughput gene silencing in plants. Methods 2003, 30, 289-295.
26. Hilson, P.; Allemeersch, J.; Altmann, T.; Aubourg, S.; Avon, A.; Beynon, J.; Bhalerao, R.P.; Bitton, F.; Caboche, M.; Cannoot, B., et al. Versatile gene-specific sequence tags for Arabidopsis functional genomics: Trancript profiling and reverse genetics applications. Genome Res. 2004, 14, 26-2189.
27. Box, M.S.; Coustham, V.; Dean, C.; Mylne, J.S. Protocol: A simple phenol-based method for 96-well extraction of high quality RNA from Arabidopsis. Plant Methods 2011, 7, 7.
28. Mallona, I.; Lischewsky, S.; Weiss, J.; Hause, B.; Egea-Cortines, M. Validation of reference genes for quantitative real-time PCR during leaf and flower development in Petunia hybrida. BMC Plant Biol. 2010, 10, 4.
29. Pfaffl, M.W.; Tichopad, A.; Prgomet, C.; Neuvians, T.P. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper—Excel-based tool using pair-wise correlations. Biotechnol. Lett. 2004, 26, 509-515.
30. Andersen, C.L.; Jensen, J.L.; Orntoft, T.F. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004, 64, 5245-5250.
31. Vandesompele, J.; De Preter, K.; Pattyn, F.; Poppe, B.; Van Roy, N.; De Paepe, A.; Speleman, F. Accurate normalization of realtime quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3, RESEARCH0034.
32. Silver, N.; Best, S.; Jiang, J.; Thein, S.L. Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol. Biol. 2006, 7, 33.
33. Xie, F.; Xiao, P.; Chen, D.; Xu, L.; Zhang, B. miRDeepFinder: A miRNA analysis tool for deep sequencing of plant small RNAs. Plant Mol. Biol. 2012, 80, 75-84.
34. Schmittgen, T.D.; Livak, K.J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 2008, 3, 1101-1108.
35. Mallona, I.; Weiss, J.; Egea-Cortines, M. pcrEfficiency: A Web tool for PCR amplification efficiency prediction. BMC Bioinform. 2011, 12, 404.
36. Navarro, P.J.; Pérez, F.; Weiss, J.; Egea-Cortines, M. Machine learning and computer vision system for phenotype data acquisition and analysis in plants. Sensors 2016, 16, 641.
37. Kahm, M.; Hasenbrink, G.; Ludwig, J. Grofit: Fitting Biological Growth Curves with R. J. Stat. Softw. 2010, 33, 1-21.
38. Ruiz-Hernández, V.; Roca, M.J.; Egea-Cortines, M.; Weiss, J. A comparison of semi-quantitative methods suitable for establishing volatile profiles. Plant Methods 2018, 14, 67.
39. Hughes, M.E.; Hogenesch, J.B.; Kornacker, K. JTK_CYCLE: An efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J. Biol. Rhythm. 2010, 25, 372-380.
40. Wu, G.; Anafi, R.C.; Hughes, M.E.; Kornacker, K.; Hogenesch, J.B. MetaCycle: An integrated R package to evaluate periodicity in large scale data. Bioinformatics 2016, 32, 3351-3353.
41. Wickham, H. Ggplot2: Elegant Graphics for Data Analysis; Springer: Berlin/Heidelberg, Germany, 2016; ISBN 978-3-319-24277-4.
42. Garnier, S.; Ross, N.; Rudis, B.; Sciaini, M.; Scherer, C. Viridis: Default Color Maps from “Matplotlib”; R Project: Vienna, Austria, 2018; R Package Version 0.5; Available online: Https://cran.r-project.org/web/packages/viridis/index.html (accessed on 11 April 2019).
43. Kubota, A.; Kita, S.; Ishizaki, K.; Nishihama, R.; Yamato, K.T.; Kohchi, T. Co-option of a photoperiodic growth-phase transition system during land plant evolution. Nat. Commun. 2014, 5, 3668.
44. Yon, F.; Seo, P.-J.; Ryu, J.Y.; Park, C.-M.; Baldwin, I.T.; Kim, S.-G. Identification and characterization of circadian clock genes in a native tobacco, Nicotiana attenuata. BMC Plant Biol. 2012, 12, 172.
45. Somers, D.E.; Schultz, T.F.; Milnamow, M.; Kay, S.A. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 2000, 101, 319-329.
46. Navarro, P.J.; Fernández, C.; Weiss, J.; Egea-Cortines, M. Development of a configurable growth chamber with a vision system to study circadian rhythm in plants. Sensors 2012, 12, 15356-15375.
47. Nusinow, D.A.; Helfer, A.; Hamilton, E.E.; King, J.J.; Imaizumi, T.; Schultz, T.F.; Farré, E.M.; Kay, S.A.; Farre, E.M. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 2011, 475, 398.
48. Amrad, A.; Moser, M.; Mandel, T.; de Vries, M.; Schuurink, R.C.; Freitas, L.; Kuhlemeier, C. Gain and Loss of Floral Scent Production through Changes in Structural Genes during Pollinator-Mediated Speciation. Curr. Biol. 2016, 26, 3303-3312.
49. Endo, M. Tissue-specific circadian clocks in plants. Curr. Opin. Plant Biol. 2016, 29, 44-49.
50. Weiss, J.; Terry, M.I.; Martos-Fuentes, M.; Letourneux, L.; Ruiz-hernández, V.; Fernández, J.A.; Egea-cortines, M. Diel pattern of circadian clock and storage protein gene expression in leaves and during seed filling in cowpea (Vigna unguiculata). BMC Plant Biol. 2018, 18, 33-53.
51. De Mairan, J.-J. Observation Botanique; Histoire de l’Académie Royale des Sciences Paris; Institut de France: Paris, France, 1729; p. 35.
52. Ku, L.; Wei, X.; Zhang, S.; Zhang, J.; Guo, S.; Chen, Y. Cloning and Characterization of a Putative TAC1 Ortholog Associated with Leaf Angle in Maize (Zea mays L.). PLoS ONE 2011, 6, e20621.
53. Kao, W.-Y.; Tsai, T.-T. Tropic leaf movements, photosynthetic gas exchange, leaf δ13C and chlorophyll a fluorescence of three soybean species in response to water availability. Plant Cell Environ. 1998, 21, 1055-1062.
54. Park, D.H. Control of Circadian Rhythms and Photoperiodic Flowering by the Arabidopsis GIGANTEA Gene. Science 1999, 285, 1579-1582.
55. Doyle, M.R.; Davis, S.J.; Bastow, R.M.; McWatters, H.G.; Kozma-Bognar, L.; Nagy, F.; Millar, A.J.; Amasino, R.M. The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 2002, 419, 74-77.
56. Kennaway, R.; Coen, E.; Green, A.; Bangham, A. Generation of diverse biological forms through combinatorial interactions between tissue polarity and growth. PLoS Comput. Biol. 2011, 7, e1002071.
57. Beemster, G.T.S.; De Vusser, K.; De Tavernier, E.; De Bock, K.; Inze, D. Variation in growth rate between Arabidopsis ecotypes is correlated with cell division and A-type cyclin-dependent kinase activity. Plant Physiol. 2002, 129, 854-864.
58. Feys, K.; Demuynck, K.; De Block, J.; Bisht, A.; De Vliegher, A.; Inzé, D.; Nelissen, H. Growth rate rather than growth duration drives growth heterosis in maize B104 hybrids. Plant Cell Environ. 2017, 41, 374-382.
59. Thain, S.C.; Murtas, G.; Lynn, J.R.; McGrath, R.B.; Millar, A.J. The circadian clock that controls gene expression in Arabidopsis is tissue specific. Plant Physiol. 2002, 130, 102-110.
60. Bordage, S.; Sullivan, S.; Laird, J.; Millar, A.J.; Nimmo, H.G. Organ specificity in the plant circadian system is explained by different light inputs to the shoot and root clocks. New Phytol. 2016, 212, 136-149.
61. Voß, U.; Wilson, M.H.; Kenobi, K.; Gould, P.D.; Robertson, F.C.; Peer, W.A.; Lucas, M.; Swarup, K.; Casimiro, I.; Holman, T.J., et al. The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nat. Commun. 2015, 6, 7641.
62. Farré, E.M. The regulation of plant growth by the circadian clock. Plant Biol. 2012, 14, 401-410.
63. Fung-Uceda, J.; Lee, K.; Seo, P.J.; Polyn, S.; De Veylder, L.; Mas, P. The Circadian Clock Sets the Time of DNA Replication Licensing to Regulate Growth in Arabidopsis. Dev. Cell 2018, 45, 101-113.
64. Hoballah, M.E.; Stuurman, J.; Turlings, T.C.J.; Guerin, P.M.; Connétable, S.; Kuhlemeier, C.; Connetable, S.; Kuhlemeier, C. The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta. Planta 2005, 222, 141-150.
65. Unsicker, S.B.; Kunert, G.; Gershenzon, J. Protective perfumes: The role of vegetative volatiles in plant defense against herbivores. Curr. Opin. Plant Biol. 2009, 12, 479-485.
66. Pichersky, E.; Gershenzon, J. The formation and function of plant volatiles: Perfumes for pollinator attraction and defense. Curr. Opin. Plant Biol. 2002, 5, 237-243.
67. Junker, R.R.; Blüthgen, N. Floral scents repel potentially nectar-thieving ants. Evol. Ecol. Res. 2008, 10, 295-308.
68. Aharoni, A. Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants. Plant Cell Online 2003, 15, 2866-2884.
69. Yon, F.; Kessler, D.; Joo, Y.; Cortés Llorca, L.; Kim, S.G.; Baldwin, I.T. Fitness consequences of altering floral circadian oscillations for Nicotiana attenuata. J. Integr. Plant Biol. 2017, 59, 180-189.
70. Bhatia, V.; Maisnam, J.; Jain, A.; Sharma, K.K.; Bhattacharya, R. Aphid-repellent pheromone E-β-farnesene is generated in transgenic Arabidopsis thaliana over-expressing farnesyl diphosphate synthase2. Ann. Bot. 2015, 115, 581-591.