A versatile phenotyping system and analytics platform reveals diverse temporal responses to water availability in Setaria

Molecular Plant

Volumn 8, Issue 10, 2015, Pages 1520-1535

  Fahlgren, Noah ^a   Feldman, Maximilian ^a   Gehan, Malia A ^a   Wilson, Melinda S ^a   Shyu, Christine ^a   Bryant, Douglas W ^a   Hill, Steven T ^a   McEntee, Colton J ^a   Warnasooriya, Sankalpi N ^a   Kumar, Indrajit ^a   Ficor, Tracy ^a   Turnipseed, Stephanie ^a   Gilbert, Kerrigan B ^a   Brutnell, Thomas P ^a   Carrington, James C ^a   Mockler, Todd C ^a   Baxter, Ivan ^b  

^a DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

abiotic environmental stress; bioinformatics; development; phenotyping; water relations

Indexed keywords

WATER;

BIOLOGY; METABOLISM; PHENOTYPE; SETARIA (PLANT);

COMPUTATIONAL BIOLOGY; PHENOTYPE; SETARIA PLANT; WATER;

EID: 84943450041     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2015.06.005     Document Type: Article

References (87)

1. M.D. Abràmoff, P.J. Magalhães, and S.J. Ram Image processing with ImageJ Biophotonics Int. 11 2004 36 43
2. D. Adler, and D. Murdoch rgl: 3D Visualization Device System R Package 2014 version 0.93 1098
3. V. Albrecht-Borth, D. Kauss, D. Fan, Y. Hu, D. Collinge, S. Marri, M. Liebers, K. Apel, T. Pfannschmidt, W.S. Chow, and et al. A novel proteinase, SNOWY COTYLEDON4, is required for photosynthetic acclimation to higher light intensities in Arabidopsis Plant Physiol. 163 2013 732 745
4. P. Andrade-Sanchez, M.A. Gore, J.T. Heun, K.R. Thorp, A.E. Carmo-Silva, A.N. French, M.E. Salvucci, and J.W. White Development and evaluation of a field-based high-throughput phenotyping platform Funct. Plant Biol. 41 2014 68 79
5. B. Auguie gridExtra: Functions in Grid Graphics R Package 2012 version 0.91
6. D. Bates, M. Mächler, B. Bolker, and S. Walker Fitting Linear Mixed-Effects Models Using lme4 arXiv preprint 2014 arXiv:1406.5823
7. P.N. Benfey, and T. Mitchell-Olds From genotype to phenotype: systems biology meets natural variation Science 320 2008 495 497
8. J.L. Bennetzen, J. Schmutz, H. Wang, R. Percifield, J. Hawkins, A.C. Pontaroli, M. Estep, L. Feng, J.N. Vaughn, J. Grimwood, and et al. Reference genome sequence of the model plant Setaria Nat. Biotechnol. 30 2012 555 561
9. B. Berger, B. Parent, and M. Tester High-throughput shoot imaging to study drought responses J. Exp. Bot. 61 2010 3519 3528
10. H. Bozdogan Model selection and Akaike's Information Criterion (AIC): the general theory and its analytical extensions Psychometrika 52 1987 345 370
11. G. Bradski The opencv library Doctor Dobbs J. 25 2000 120 126
12. E.A. Bray Plant responses to water deficit Trends Plant Sci. 2 1997 48 54
13. T.P. Brutnell, L. Wang, K. Swartwood, A. Goldschmidt, D. Jackson, X.-G. Zhu, E. Kellogg, and J. Van Eck Setaria viridis: a model for C4 photosynthesis Plant Cell 22 2010 2537 2544
14. G.A. Carter Primary and secondary effects of water content on the spectral reflectance of leaves Am. J. Bot. 78 1991 916
15. H. Chen VennDiagram: Generate High-Resolution Venn and Euler Plots BMC Bioinformatics 2014 35
16. A. Dabney, and J.D. Storey qvalue: Q-Value Estimation for False Discovery Rate Control R Package 2015 version 1.26.0
17. H. Darmency, C. Ouin, and J. Pernes Breeding foxtail millet (Setaria italica) for quantitative traits after interspecific hybridization and polyploidization Genome 29 1987 453 456
18. K.M. Devos, Z.M. Wang, J. Beales, T. Sasaki, and M.D. Gale Comparative genetic maps of foxtail millet (Setaria italica) and rice (Oryza sativa) Theor. Appl. Genet. 96 1998 63 68
19. A.N. Doust Architectural evolution and its implications for domestication in grasses Ann. Bot. 100 2007 941 950
20. A.N. Doust Grass architecture: genetic and environmental control of branching Curr. Opin. Plant Biol. 10 2007 21 25
21. A.N. Doust, and E.A. Kellogg Effect of genotype and environment on branching in weedy green millet (Setaria viridis) and domesticated foxtail millet (Setaria italica) (Poaceae) Mol. Ecol. 15 2006 1335 1349
22. A.N. Doust, E.A. Kellogg, K.M. Devos, and J.L. Bennetzen Foxtail millet: a sequence-driven grass model system Plant Physiol. 149 2009 137 141
23. J.T. Dudley, and A.J. Butte A quick guide for developing effective bioinformatics programming skills PLoS Comput. Biol. 5 2009 e1000589
24. N. Fahlgren, M.A. Gehan, and I. Baxter Lights, camera, action: high-throughput plant phenotyping is ready for a close-up Curr. Opin. Plant Biol. 24 2015 93 99
25. N. Fernández-García, E. Olmos, E. Bardisi, J. García-De la Garma, C. López-Berenguer, and J.S. Rubio-Asensio Intrinsic water use efficiency controls the adaptation to high salinity in a semi-arid adapted plant, henna (Lawsonia inermis L.) J. Plant Physiol. 171 2014 64 75
26. M. Fourment, and M.R. Gillings A comparison of common programming languages used in bioinformatics BMC Bioinformatics 9 2008 82
27. J. Fox, and S. Weisberg An R Companion to Applied Regression 2nd edn 2011 SAGE Publications
28. R.T. Furbank, and M. Tester Phenomics-technologies to relieve the phenotyping bottleneck Trends Plant Sci. 16 2011 635 644
29. A.K. Garg, J.-K. Kim, T.G. Owens, A.P. Ranwala, Y.D. Choi, L.V. Kochian, and R.J. Wu Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses Proc. Natl. Acad. Sci. USA 99 2002 15898 15903
30. R.C. Gentleman, V.J. Carey, D.M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, J. Gentry, and et al. Bioconductor: open software development for computational biology and bioinformatics Genome Biol. 5 2004 R80
31. A. Genz, and F. Bretz Computation of Multivariate Normal and t Probabilities Vol. 195 2009 Springer Science & Business Media
32. A. Genz, F. Bretz, T. Miwa, X. Mi, F. Leisch, F. Scheipl, and T. Hothorn mvtnorm: Multivariate Normal and t Distributions R Package 2014 version 0.9-2
33. P. Gerland, A.E. Raftery, H. Sevcikova, N. Li, D. Gu, T. Spoorenberg, L. Alkema, B.K. Fosdick, J. Chunn, N. Lalic, and et al. World population stabilization unlikely this century Science 346 2014 234 237
34. D. Gilbert Bioinformatics software resources Brief. Bioinform. 5 2004 300 304
35. S.A. Goff, M. Vaughn, S. McKay, E. Lyons, A.E. Stapleton, D. Gessler, N. Matasci, L. Wang, M. Hanlon, A. Lenards, and et al. The iPlant Collaborative: cyberinfrastructure for plant biology Front. Plant Sci. 2 2011 34
36. M.R. Golzarian, R.A. Frick, K. Rajendran, B. Berger, S. Roy, M. Tester, and D.S. Lun Accurate inference of shoot biomass from high-throughput images of cereal plants Plant Methods 7 2011 2
37. G. Grolemund, and H. Wickham Dates and times made easy with lubridate J. Stat. Softw. 40 2011 1 25
38. A. Hartmann, T. Czauderna, R. Hoffmann, N. Stein, and F. Schreiber HTPheno: an image analysis pipeline for high-throughput plant phenotyping BMC Bioinformatics 12 2011 148
39. N. Honsdorf, T.J. March, B. Berger, M. Tester, and K. Pillen High-throughput phenotyping to detect drought tolerance QTL in wild barley introgression lines PLoS One 9 2014 e97047
40. J.D. Hunter Matplotlib: a 2D graphics environment Comput. Sci. Eng. 9 2007 90 95
41. IPCC Climate change 2014: impacts, adaptation, and vulnerability Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change 2014 Cambridge University Press Cambridge and New York, NY
42. G. Jia, X. Huang, H. Zhi, Y. Zhao, Q. Zhao, W. Li, Y. Chai, L. Yang, K. Liu, and H. Lu A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica) Nat. Genet. 45 2013 957 961
43. E.A. Kellogg Phylogenetic aspects of the evolution of C4 photosynthesis R.F. Sage, R.K. Monson, C4 Plant Biology 1999 Academic Press San Diego, CA 411 444
44. C. Klukas, D. Chen, and J.-M. Pape Integrated analysis platform: an open-source information system for high-throughput plant phenotyping Plant Physiol. 165 2014 506 518
45. D. Kremnev, and Å. Strand Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis Front. Plant Sci. 5 2014 385
46. H.-H. Kunz, M. Gierth, A. Herdean, M. Satoh-Cruz, D.M. Kramer, C. Spetea, and J.I. Schroeder Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis Proc. Natl. Acad. Sci. USA 111 2014 7480 7485
47. K. Kvilekval, D. Fedorov, B. Obara, A. Singh, and B.S. Manjunath Bisque: a platform for bioimage analysis and management Bioinformatics 26 2010 544 552
48. C. Lata, P.P. Sahu, and M. Prasad Comparative transcriptome analysis of differentially expressed genes in foxtail millet (Setaria italica L.) during dehydration stress Biochem. Biophys. Res. Commun. 393 2010 720 727
49. C. Lata, S. Bhutty, R.P. Bahadur, M. Majee, and M. Prasad Association of an SNP in a novel DREB2-like gene SiDREB2 with stress tolerance in foxtail millet (Setaria italica L.) J. Exp. Bot. 62 2011 3387 3401
50. P. Li, and T.P. Brutnell Setaria viridis and Setaria italica, model genetic systems for the Panicoid grasses J. Exp. Bot. 62 2011 3031 3037
51. G. Lobet, X. Draye, and C. Périlleux An online database for plant image analysis software tools Plant Methods 9 2013 38
52. S. Mahfoozi Developmental regulation of low-temperature tolerance in winter wheat Ann. Bot. 87 2001 751 757
53. H. Mangalam The Bio∗toolkits - a brief overview Brief. Bioinform. 3 2002 296 302
54. K. Maxwell, and G.N. Johnson Chlorophyll fluorescence - a practical guide J. Exp. Bot. 51 2000 659 668
55. S. McCouch, G.J. Baute, J. Bradeen, P. Bramel, P.K. Bretting, E. Buckler, J.M. Burke, D. Charest, S. Cloutier, G. Cole, and et al. Agriculture: feeding the future Nature 499 2013 23 24
56. B.-H. Mevik, R. Wehrens, and K.H. Liland pls: Partial Least Squares and Principal Component Regression R Package 2013 version 2
57. R. Munns, and M. Tester Mechanisms of salinity tolerance Annu. Rev. Plant Biol. 59 2008 651 681
58. E.H. Neilson, A.M. Edwards, C.K. Blomstedt, B. Berger, B.L. Moller, and R.M. Gleadow Utilization of a high-throughput shoot imaging system to examine the dynamic phenotypic responses of a C4 cereal crop plant to nitrogen and water deficiency over time J. Exp. Bot. 66 2015 1817 1832
59. T. Nelson, and N. Dengler Leaf vascular pattern formation Plant Cell 9 1997 1121 1135
60. T.E. Oliphant Python for scientific computing Comput. Sci. Eng. 9 2007 10 20
61. C.E.T. Paine, T.R. Marthews, D.R. Vogt, D. Purves, M. Rees, A. Hector, and L.A. Turnbull How to fit nonlinear plant growth models and calculate growth rates: an update for ecologists Methods Ecol. Evol. 3 2012 245 256
62. A. Paproki, X. Sirault, S. Berry, R. Furbank, and J. Fripp A novel mesh processing based technique for 3D plant analysis BMC Plant Biol. 12 2012 63
63. J. Peñuelas, and I. Filella Visible and near-infrared reflectance techniques for diagnosing plant physiological status Trends Plant Sci. 3 1998 151 156
64. J. Phattaralerphong, and H. Sinoquet A method for 3D reconstruction of tree crown volume from photographs: assessment with 3D-digitized plants Tree Physiol. 25 2005 1229 1242
65. J. Pinheiro, D. Bates, S. DebRoy, D. Sarkar, and T.R.C. Team nlme: Linear and Nonlinear Mixed Effects Models R Package 2014 version 3
66. L. Qie, G. Jia, W. Zhang, J. Schnable, Z. Shang, W. Li, B. Liu, M. Li, Y. Chai, and H. Zhi Mapping of quantitative trait locus (QTLs) that contribute to germination and early seedling drought tolerance in the interspecific cross Setaria italica×Setaria viridis PLoS One 9 2014 e101868
67. D.K. Ray, N.D. Mueller, P.C. West, and J.A. Foley Yield trends are insufficient to double global crop production by 2050 PLoS One 8 2013 e66428
68. R Core Team R: A Language and Environment for Statistical Computing 2014
69. R. Richards, and N. Thurling Variation between and within species of rapeseed (Brassica campestris and B. napus) in response to drought stress. I. Sensitivity at different stages of development Aust. J. Agric. Res. 29 1978 469
70. R.F. Sage, and X.-G. Zhu Exploiting the engine of C(4) photosynthesis J. Exp. Bot. 62 2011 2989 3000
71. D. Sarkar Lattice: Multivariate Data Visualization with R Springer Science & Business Media 2008
72. M. Satou, H. Enoki, A. Oikawa, D. Ohta, K. Saito, T. Hachiya, H. Sakakibara, M. Kusano, A. Fukushima, K. Saito, and et al. Integrated analysis of transcriptome and metabolome of Arabidopsis albino or pale green mutants with disrupted nuclear-encoded chloroplast proteins Plant Mol. Biol. 85 2014 411 428
73. F. Schoffl Regulation of the heat-shock response Plant Physiol. 117 1998 1135 1141
74. H.-D. Seelig, A. Hoehn, L.S. Stodieck, D.M. Klaus, W.W. Adams III, and W.J. Emery The assessment of leaf water content using leaf reflectance ratios in the visible, near-, and short-wave-infrared Int. J. Remote Sens. 29 2008 3701 3713
75. H.-D. Seelig, A. Hoehn, L.S. Stodieck, D.M. Klaus, W.W. Adams, and W.J. Emery Plant water parameters and the remote sensing R 1300/R 1450 leaf water index: controlled condition dynamics during the development of water deficit stress Irrig. Sci. 27 2009 357 365
76. G.L. Simpson Analogue methods in palaeoecology: using the analogue package J. Stat. Softw. 22 2007 1 29
77. S. Talukder, M. Babar, K. Vijayalakshmi, J. Poland, P. Prasad, R. Bowden, and A. Fritz Mapping QTL for the traits associated with heat tolerance in wheat (Triticum aestivum L.) BMC Genet. 15 2014 97
78. S. Urbanek, and Y. Rubner emdist: Earth Mover's Distance R Package 2012
79. W.N. Venables, and B.D. Ripley Modern Applied Statistics with S 4th edn 2002 Springer New York
80. Z.M. Wang, K.M. Devos, C.J. Liu, R.Q. Wang, and M.D. Gale Construction of RFLP-based maps of foxtail millet, Setaria italica (L.) P. Beauv Theor. Appl. Genet. 96 1998 31 36
81. S.N. Warnasooriya, and T.P. Brutnell Enhancing the productivity of grasses under high-density planting by engineering light responses: from model systems to feedstocks J. Exp. Bot. 65 2014 2825 2834
82. J.W. White, P. Andrade-Sanchez, M.A. Gore, K.F. Bronson, T.A. Coffelt, M.M. Conley, K.A. Feldmann, A.N. French, J.T. Heun, D.J. Hunsaker, and et al. Field-based phenomics for plant genetics research Field Crops Res. 133 2012 101 112
83. H. Wickham ggplot2: Elegant Graphics for Data Analysis Springer Science & Business Media 2009
84. H. Wickham The split-apply-combine strategy for data J. Stat. Softw. 40 2011 1 29
85. H. Wickham scales: Scale Functions for Graphics R package 2014
86. O. Wilkins, K. Bräutigam, and M.M. Campbell Time of day shapes Arabidopsis drought transcriptomes Plant J. 63 2010 715 727
87. J. Zhang, T. Liu, J. Fu, Y. Zhu, J. Jia, J. Zheng, Y. Zhao, Y. Zhang, and G. Wang Construction and application of EST library from Setaria italica in response to dehydration stress Genomics 90 2007 121 131