Gene expression plasticity resulting from parental leaf damage in Mimulus guttatus

New Phytologist

Volumn 205, Issue 2, 2015, Pages 894-906

  Colicchio, Jack M ^a   Monnahan, Patrick J ^a   Kelly, John K ^a   Hileman, Lena C ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

Epigenetics; Mimulus guttatus; Plant stress response; RNA seq; Transcriptome; Transgenerational plasticity; Trichomes

Indexed keywords

MIMULUS GUTTATUS;

GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETIC EPIGENESIS; GENETICS; METABOLISM; MIMULUS; PHYSIOLOGY; PLANT LEAF; SEEDLING;

EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; GENE ONTOLOGY; METABOLIC NETWORKS AND PATHWAYS; MIMULUS; PLANT LEAVES; SEEDLING;

EID: 84919667500     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13081     Document Type: Article

References (74)

1. Agrawal AA. 2002. Herbivory and maternal effects: mechanisms and consequences of transgenerational induced plant resistance. Ecology 83: 3408-3415.
2. Agrawal AA, Laforsch C, Tollrian R. 1999. Transgenerational induction of defences in animals and plants. Nature 401: 60-63.
3. Ågren J, Schemske DW. 1993. The cost of defense against herbivores: an experimental study of trichome production in Brassica rapa. The American Naturalist 141: 338-350.
4. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology 11: R106.
5. Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K. 2004. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. The Plant Cell 16: 3460-3479.
6. Applequist WL, Cronn R, Wendel JF. 2001. Comparative development of fiber in wild and cultivated cotton. Evolution & Development 3: 3-17.
7. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT. 2000. Gene ontology: tool for the unification of biology. Nature Genetics 25: 25-29.
8. Beardsley PM, Olmstead RG. 2002. Redefining Phrymaceae: the placement of Mimulus, tribe Mimuleae, and Phryma. American Journal of Botany 89: 1093-1102.
9. Bilichak A, Ilnystkyy Y, Hollunder J, Kovalchuk I. 2012. The progeny of Arabidopsis thaliana plants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression. PLoS ONE 7: e30515.
10. Bleecker AB, Kende H. 2000. Ethylene: a gaseous signal molecule in plants. Annual Review of Cell and Developmental Biology 16: 1-18.
11. Blödner C, Goebel C, Feussner I, Gatz C, Polle A. 2007. Warm and cold parental reproductive environments affect seed properties, fitness, and cold responsiveness in Arabidopsis thaliana progenies. Plant, Cell & Environment 30: 165-175.
12. Boyko A, Blevins T, Yao Y, Golubov A, Bilichak A, Ilnytskyy Y, Hollander J, Meins F Jr, Kovalchuk I. 2010. Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS ONE 5: e9514.
13. Boyko A, Kovalchuk I. 2010. Transgenerational response to stress in Arabidopsis thaliana. Plant Signaling & Behavior 5: 995-998.
14. Brock G, Pihur V, Datta S, Datta S. 2011. clValid, an R package for cluster validation. Journal of Statistical Software 25: 1-22.
15. Bruce TJ, Matthes MC, Napier JA, Pickett JA. 2007. Stressful "memories" of plants: evidence and possible mechanisms. Plant Science 173: 603-608.
16. Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, Lopes T, Gardner R, Berger F, Feijó JA, Becker JD. 2012. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151: 194-205.
17. Chinnusamy V, Gong Z, Zhu JK. 2008. Abscisic acid-mediated epigenetic processes in plant development and stress responses. Journal of Integrative Plant Biology 50: 1187-1195.
18. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
19. Cosgrove DJ. 1997. Assembly and enlargement of the primary cell wall in plants. Annual Review of Cell and Developmental Biology 13: 171-201.
20. Dixon RA, Achnine L, Kota P, Liu CJ, Reddy M, Wang L. 2002. The phenylpropanoid pathway and plant defence - a genomics perspective. Molecular Plant Pathology 3: 371-390.
21. Dudley SA, File AL. 2007. Kin recognition in an annual plant. Biology Letters 3: 435-438.
22. Eklöf JM, Brumer H. 2010. The XTH gene family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiology 153: 456-466.
23. Galloway LF, Etterson JR. 2007. Transgenerational plasticity is adaptive in the wild. Science 318: 1134-1136.
24. Gang DR, Kasahara H, Xia Z-Q, Vander Mijnsbrugge K, Bauw G, Boerjan W, Van Montagu M, Davin LB, Lewis NG. 1999. Evolution of plant defense mechanisms relationships of phenylcoumaran benzylic ether reductases to pinoresinol-lariciresinol and isoflavone reductases. Journal of Biological Chemistry 274: 7516-7527.
25. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 5: R80.
26. González-Guzmán M, Apostolova N, Bellés JM, Barrero JM, Piqueras P, Ponce MR, Micol JL, Serrano R, Rodríguez PL. 2002. The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. The Plant Cell 14: 1833-1846.
27. Gutzat R, Mittelsten Scheid O. 2012. Epigenetic responses to stress: triple defense? Current Opinion in Plant Biology 15: 568-573.
28. Hahlbrock K, Scheel D. 1989. Physiology and molecular biology of phenylpropanoid metabolism. Annual Review of Plant Biology 40: 347-369.
29. Herman JJ, Spencer HG, Donohue K, Sultan SE. 2013. How stable 'should' epigenetic modifications be? Insights from adaptive plasticity and bet hedging. Evolution 68: 632-643.
30. Holeski L. 2007. Within and between generation phenotypic plasticity in trichome density of Mimulus guttatus. Journal of Evolutionary Biology 20: 2092-2100.
31. Holeski LM, Chase-Alone R, Kelly JK. 2010. The genetics of phenotypic plasticity in plant defense: trichome production in Mimulus guttatus. The American Naturalist 175: 391-400.
32. Holeski LM, Jander G, Agrawal AA. 2012. Transgenerational defense induction and epigenetic inheritance in plants. Trends in Ecology & Evolution 27: 618-626.
33. Holeski LM, Zinkgraf MS, Couture JJ, Whitham TG, Lindroth RL. 2013. Transgenerational effects of herbivory in a group of long-lived tree species: maternal damage reduces offspring allocation to resistance traits, but not growth. Journal of Ecology 101: 1062-1073.
34. Hülskamp M, Miséra S, Jürgens G. 1994. Genetic dissection of trichome cell development in Arabidopsis. Cell 76: 555-566.
35. Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J. 2011. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472: 115-119.
36. Jablonka E. 2012. Epigenetic inheritance and plasticity: the responsive germline. Progress in Biophysics and Molecular Biology 111: 99-107.
37. Jablonka E, Raz G. 2009. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology 84: 131-176.
38. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Research 40(D1): D109-D114.
39. Korth KL, Dixon RA. 1997. Evidence for chewing insect-specific molecular events distinct from a general wound response in leaves. Plant Physiology 115: 1299-1305.
40. Langfelder P, Zhang B, Horvath S. 2008. Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinformatics 24: 719-720.
41. Lang-Mladek C, Popova O, Kiok K, Berlinger M, Rakic B, Aufsatz W, Jonak C, Hauser M-T, Luschnig C. 2010. Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Molecular Plant 3: 594-602.
42. Law CW, Chen Y, Shi W, Smyth GK. 2013a. Voom! Precision weights unlock linear model analysis tools for RNA-seq read counts: Technical Report 1 May 2013, Bioinformatics Division, Walter and Eliza Hall Institute of Medical Reseach, Melbourne, Australia. [WWW document] URL http://www.statsci.org/smyth/pubs/VoomPreprint.pdf [accessed 15 July 2014].
43. Law JA, Du J, Hale CJ, Feng S, Krajewski K, Palanca AMS, Strahl BD, Patel DJ, Jacobsen SE. 2013b. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498: 385-389.
44. Li J, Tibshirani R. 2011. Finding consistent patterns: a nonparametric approach for identifying differential expression in RNA-seq data. Statistical Methods in Medical Research 22: 519-536.
45. Lindquist S, Craig E. 1988. The heat-shock proteins. Annual Review of Genetics 22: 631-677.
46. McCue AD, Nuthikattu S, Reeder SH, Slotkin RK. 2012. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLoS Genetics 8: e1002474.
47. Mirouze M, Paszkowski J. 2011. Epigenetic contribution to stress adaptation in plants. Current Opinion in Plant Biology 14: 267-274.
48. Molinier J, Ries G, Zipfel C, Hohn B. 2006. Transgeneration memory of stress in plants. Nature 442: 1046-1049.
49. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC. 2010. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328: 872-875.
50. Mousseau TA, Fox CW. 1998. The adaptive significance of maternal effects. Trends in Ecology & Evolution 13: 403-407.
51. Pieterse CM. 2012. Prime time for transgenerational defense. Plant Physiology 158: 545.
52. Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G. 2012. Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiology 158: 854-863.
53. Richards CL, Verhoeven KJ, Bossdorf O. 2012. Evolutionary significance of epigenetic variation. In: Wendel JF, Greilhuber J, Doležel J, Leitch IJ, eds. Plant genome diversity, vol 1. Wien, Austria: Springer, 257-274.
54. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
55. Sachs MM, Ho T-HD. 1986. Alteration of gene expression during environmental stress in plants. Annual Review of Plant Physiology 37: 363-376.
56. +)-abscisic acid 8′-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiology 134: 1439-1449.
57. Scoville AG, Barnett LL, Bodbyl-Roels S, Kelly JK, Hileman LC. 2011. Differential regulation of a MYB transcription factor is correlated with transgenerational epigenetic inheritance of trichome density in Mimulus guttatus. New Phytologist 191: 251-263.
58. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K. 2001. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. The Plant Cell 13: 61-72.
59. Si-Ammour A, Windels D, Arn-Bouldoires E, Kutter C, Ailhas J, Meins F, Vazquez F. 2011. miR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin receptor clade and auxin-related development of Arabidopsis leaves. Plant Physiology 157: 683-691.
60. Slaughter A, Daniel X, Flors V, Luna E, Hohn B, Mauch-Mani B. 2012. Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiology 158: 835-843.
61. Soneson C, Delorenzi M. 2013. A comparison of methods for differential expression analysis of RNA-seq data. BMC Bioinformatics 14: 91.
62. Sunkar R, Chinnusamy V, Zhu J, Zhu J-K. 2007. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Science 12: 301-309.
63. Swindell WR, Huebner M, Weber AP. 2007. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8: 125.
64. Tarazona S, García-Alcalde F, Dopazo J, Ferrer A, Conesa A. 2011. Differential expression in RNA-seq: a matter of depth. Genome Research 21: 2213-2223.
65. Treutter D. 2005. Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biology 7: 581-591.
66. Tsang E, Bowler C, Hérouart D, Van Camp W, Villarroel R, Genetello C, Van Montagu M, Inzé D. 1991. Differential regulation of superoxide dismutases in plants exposed to environmental stress. The Plant Cell 3: 783-792.
67. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. 2012. Primer3-new capabilities and interfaces. Nucleic Acids Research 40: e115.
68. Verhoeven KJ, Jansen JJ, van Dijk PJ, Biere A. 2010. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytologist 185: 1108-1118.
69. Verhoeven KJ, van Gurp TP. 2012. Transgenerational effects of stress exposure on offspring phenotypes in apomictic dandelion. PLoS ONE 7: e38605.
70. Walling LL. 2000. The myriad plant responses to herbivores. Journal of Plant Growth and Regulation 19: 195-216.
71. Wehrens R, Buydens LM. 2007. Self-and super-organizing maps in R: the Kohonen package. Journal of Statistical Software 21: 1-19.
72. Wink M. 1988. Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theoretical and Applied Genetics 75: 225-233.
73. Yan Y, Borrego E, Kolomiets MV. 2013. Jasmonate biosynthesis, perception and function in plant development and stress responses. In: Baez RV, ed. Lipid metabolism. Rijeka, Croatia: InTech Europe, 393-442.
74. Yu Y-B, Adams DO, Yang SF. 1979. 1-Aminocyclopropanecarboxylate synthase, a key enzyme in ethylene biosynthesis. Archives of Biochemistry and Biophysics 198: 280-286.