Genome-wide data (ChIP-seq) enabled identification of cell wall-related and aquaporin genes as targets of tomato ASR1, a drought stress-responsive transcription factor

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Ricardi, Martiniano M ^a   González, Rodrigo M ^a   Zhong, Silin ^b   Domínguez, Pía G ^c   Duffy, Tomas ^c   Turjanski, Pablo G ^d   Salgado Salter, Juan D ^a   Alleva, Karina ^e   Carrari, Fernando ^c   Giovannoni, James J ^f   Estévez, José M ^a   Iusem, Norberto D ^a,d  

^a INSTITUTO DE FISIOLOGÍA   (Argentina)

^b United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^c INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

^d UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^e Ciudad Autónoma de Buenos Aires   (Argentina)

^f Department of Obstetrics Gynecology   (United States)

Author keywords

Aquaporin; ASR1; Cell wall; ChIP seq; Tomato; Water stress

Indexed keywords

ARABIDOPSIS; LYCOPERSICON ESCULENTUM;

AQUAPORIN; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ARTICLE; CELL WALL; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; TOMATO;

AQUAPORINS; CELL WALL; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; PLANT PROTEINS; TRANSCRIPTION FACTORS;

EID: 84892393715     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-29     Document Type: Article

References (65)

1. Cominelli E, Conti L, Tonelli C, Galbiati M. Challenges and perspectives to improve crop drought and salinity tolerance. N Biotechnol 2013, 30(4):355-361. 10.1016/j.nbt.2012.11.001, 23165101.
2. Qiu YL, Palmer JD. Phylogeny of early land plants: insights from genes and genomes. Trends Plant Sci 1999, 4(1):26-30. 10.1016/S1360-1385(98)01361-2, 10234267.
3. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y, et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 2008, 319(5859):64-69. 10.1126/science.1150646, 18079367.
4. Dure L, Greenway SC, Galau GA. Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis. Biochemistry 1981, 20(14):4162-4168. 10.1021/bi00517a033, 7284317.
5. Tunnacliffe A, Wise MJ. The continuing conundrum of the LEA proteins. Naturwissenschaften 2007, 94(10):791-812. 10.1007/s00114-007-0254-y, 17479232.
6. Caramelo JJ, Iusem ND. When cells lose water: Lessons from biophysics and molecular biology. Prog Biophys Mol Biol 2009, 99(1):1-6. 10.1016/j.pbiomolbio.2008.10.001, 18977383.
7. Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA. The enigmatic LEA proteins and other hydrophilins. Plant Physiol 2008, 148(1):6-24. 10.1104/pp.108.120725, 2528095, 18772351.
8. Frankel N, Hasson E, Iusem ND, Rossi MS. Adaptive evolution of the water stress-induced gene Asr2 in Lycopersicon species dwelling in arid habitats. Mol Biol Evol 2003, 20(12):1955-1962. 10.1093/molbev/msg214, 12949146.
9. Giombini MI, Frankel N, Iusem ND, Hasson E. Nucleotide polymorphism in the drought responsive gene Asr2 in wild populations of tomato. Genetica 2009, 136(1):13-25. 10.1007/s10709-008-9295-1, 18636230.
10. Iusem ND, Bartholomew DM, Hitz WD, Scolnik PA. Tomato (Lycopersicon esculentum) transcript induced by water deficit and ripening. Plant Physiol 1993, 102(4):1353-1354. 10.1104/pp.102.4.1353, 158931, 8278555.
11. Konrad Z, Bar-Zvi D. Synergism between the chaperone-like activity of the stress regulated ASR1 protein and the osmolyte glycine-betaine. Planta 2008, 227(6):1213-1219. 10.1007/s00425-008-0693-5, 18270732.
12. Maskin L, Frankel N, Gudesblat G, Demergasso MJ, Pietrasanta LI, Iusem ND. Dimerization and DNA-binding of ASR1, a small hydrophilic protein abundant in plant tissues suffering from water loss. Biochem Biophys Res Commun 2007, 352(4):831-835. 10.1016/j.bbrc.2006.11.115, 17157822.
13. Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R. A grape ASR protein involved in sugar and abscisic acid signaling. Plant Cell 2003, 15(9):2165-2180. 10.1105/tpc.013854, 181338, 12953118.
14. Shkolnik D, Bar-Zvi D. Tomato ASR1 abrogates the response to abscisic acid and glucose in Arabidopsis by competing with ABI4 for DNA binding. Plant Biotechnol J 2008, 6(4):368-378. 10.1111/j.1467-7652.2008.00328.x, 18363631.
15. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, et al. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 2002, 31(3):279-292. 10.1046/j.1365-313X.2002.01359.x, 12164808.
16. Gazanchian A, Hajheidari M, Sima NK, Salekdeh GH. Proteome response of Elymus elongatum to severe water stress and recovery. J Exp Bot 2007, 58(2):291-300.
17. The-Tomato-Genome-Consortium The tomato genome sequence provides insights into fleshy fruit evolution. Nature 2012, 485(7400):635-641. 10.1038/nature11119, 3378239, 22660326, The-Tomato-Genome-Consortium.
18. Infante CR, Park S, Mihala AG, Kingsley DM, Menke DB. Pitx1 broadly associates with limb enhancers and is enriched on hindlimb cis-regulatory elements. Dev Biol 2013, 374(1):234-244. 10.1016/j.ydbio.2012.11.017, 3640454, 23201014.
19. Zhang JX, Zhang J, Yan W, Wang YY, Han L, Yue X, Liu N, You YP, Jiang T, Pu PY, et al. Unique genome-wide map of TCF4 and STAT3 targets using ChIP-seq reveals their association with new molecular subtypes of glioblastoma. Neuro Oncol 2013, 15(3):279-289. 10.1093/neuonc/nos306, 23295773.
20. Muino JM, Angenent GC, Kaufmann K. Visualizing and characterizing in vivo DNA-binding events and direct target genes of plant transcription factors. Methods Mol Biol 2011, 754:293-305. 10.1007/978-1-61779-154-3_17, 21720960.
21. Feng J, Liu T, Qin B, Zhang Y, Liu XS. Identifying ChIP-seq enrichment using MACS. Nat Protoc 2012, 7(9):1728-1740. 10.1038/nprot.2012.101, 3868217, 22936215.
22. Thorvaldsdottir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2013, 14(2):178-192. 10.1093/bib/bbs017, 3603213, 22517427.
23. Ji H, Jiang H, Ma W, Wong WH, et al. Using CisGenome to Analyze ChIP-Chip and ChIP-seq Data. Current Protocols in Bioinformatics 2011, Hoboken, New Jersey, USA: Wiley Online Library, Baxevanis AD, 2, Unit 2.13.
24. Muino JM, Kaufmann K, van Ham RC, Angenent GC, Krajewski P. ChIP-seq Analysis in R (CSAR): an R package for the statistical detection of protein-bound genomic regions. Plant Methods 2011, 7:11. 10.1186/1746-4811-7-11, 3114017, 21554688.
25. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004, 37(6):914-939. 10.1111/j.1365-313X.2004.02016.x, 14996223.
26. van Heeringen SJ, Veenstra GJ. GimmeMotifs: a de novo motif prediction pipeline for ChIP-sequencing experiments. Bioinformatics 2011, 27(2):270-271. 10.1093/bioinformatics/btq636, 3018809, 21081511.
27. Zhu W, Ouyang S, Iovene M, O'Brien K, Vuong H, Jiang J, Buell CR. Analysis of 90 Mb of the potato genome reveals conservation of gene structures and order with tomato but divergence in repetitive sequence composition. BMC Genomics 2008, 9(1):286. 10.1186/1471-2164-9-286, 2442093, 18554403.
28. Frankel N, Nunes-Nesi A, Balbo I, Mazuch J, Centeno D, Iusem ND, Fernie AR, Carrari F. ci21A/Asr1 expression influences glucose accumulation in potato tubers. Plant Mol Biol 2007, 63(5):719-730. 10.1007/s11103-006-9120-0, 17211513.
29. Landt SG, Marinov GK, Kundaje A, Kheradpour P, Pauli F, Batzoglou S, Bernstein BE, Bickel P, Brown JB, Cayting P, et al. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 2011, 22(9):1813-1831.
30. Ji H, Jiang H, Ma W, Johnson DS, Myers RM, Wong WH. An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat Biotechnol 2008, 26(11):1293-1300. 10.1038/nbt.1505, 2596672, 18978777.
31. Aoki K, Yano K, Suzuki A, Kawamura S, Sakurai N, Suda K, Kurabayashi A, Suzuki T, Tsugane T, Watanabe M, et al. Large-scale analysis of full-length cDNAs from the tomato (Solanum lycopersicum) cultivar Micro-Tom, a reference system for the Solanaceae genomics. BMC Genomics 2010, 11:210. 10.1186/1471-2164-11-210, 2859864, 20350329.
32. Ritter DI, Dong Z, Guo S, Chuang JH. Transcriptional enhancers in protein-coding exons of vertebrate developmental genes. PLoS One 2012, 7(5):e35202. 10.1371/journal.pone.0035202, 3342275, 22567096.
33. Moore JP, Vicre-Gibouin M, Farrant JM, Driouich A. Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plant 2008, 134(2):237-245. 10.1111/j.1399-3054.2008.01134.x, 18494857.
34. Maurel C, Verdoucq L, Luu DT, Santoni V. Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 2008, 59:595-624. 10.1146/annurev.arplant.59.032607.092734, 18444909.
35. Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R. Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 2001, 125(3):1206-1215. 10.1104/pp.125.3.1206, 65601, 11244102.
36. Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysse L, Weig AR, Kjellbom P. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 2001, 126(4):1358-1369. 10.1104/pp.126.4.1358, 117137, 11500536.
37. Danielson JA, Johanson U. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 2008, 8:45. 10.1186/1471-2229-8-45, 2386804, 18430224.
38. Jang JY, Kim DG, Kim YO, Kim JS, Kang H. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 2004, 54(5):713-725.
39. Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P. Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 2005, 59(3):469-484. 10.1007/s11103-005-0352-1, 16235111.
40. Lian HL, Yu X, Lane D, Sun WN, Tang ZC, Su WA. Upland rice and lowland rice exhibited different PIP expression under water deficit and ABA treatment. Cell Res 2006, 16(7):651-660. 10.1038/sj.cr.7310068, 16773042.
41. Secchi F, Lovisolo C, Uehlein N, Kaldenhoff R, Schubert A. Isolation and functional characterization of three aquaporins from olive (Olea europaea L.). Planta 2007, 225(2):381-392.
42. Li GW, Peng YH, Yu X, Zhang MH, Cai WM, Sun WN, Su WA. Transport functions and expression analysis of vacuolar membrane aquaporins in response to various stresses in rice. J Plant Physiol 2008, 165(18):1879-1888. 10.1016/j.jplph.2008.05.002, 18707797.
43. Lopez D, Bronner G, Brunel N, Auguin D, Bourgerie S, Brignolas F, Carpin S, Tournaire-Roux C, Maurel C, Fumanal B, et al. Insights into Populus XIP aquaporins: evolutionary expansion, protein functionality, and environmental regulation. J Exp Bot 2012, 63(5):2217-2230. 10.1093/jxb/err404, 22223812.
44. Sarda X, Tousch D, Ferrare K, Legrand E, Dupuis JM, Casse-Delbart F, Lamaze T. Two TIP-like genes encoding aquaporins are expressed in sunflower guard cells. Plant J 1997, 12(5):1103-1111. 10.1046/j.1365-313X.1997.12051103.x, 9418051.
45. Salma N, Xiao H, Imbalzano AN. Temporal recruitment of CCAAT/enhancer-binding proteins to early and late adipogenic promoters in vivo. J Mol Endocrinol 2006, 36(1):139-151. 10.1677/jme.1.01918, 16461934.
46. Geitmann A, Ortega JK. Mechanics and modeling of plant cell growth. Trends Plant Sci 2009, 14(9):467-478. 10.1016/j.tplants.2009.07.006, 19717328.
47. Wu Y, Cosgrove DJ. Adaptation of roots to low water potentials by changes in cell wall extensibility and cell wall proteins. J Exp Bot 2000, 51(350):1543-1553. 10.1093/jexbot/51.350.1543, 11006305.
48. Levy A, Erlanger M, Rosenthal M, Epel BL. A plasmodesmata-associated beta-1,3-glucanase in Arabidopsis. Plant J 2007, 49(4):669-682. 10.1111/j.1365-313X.2006.02986.x, 17270015.
49. Ueki S, Citovsky V. Identification of an interactor of cadmium ion-induced glycine-rich protein involved in regulation of callose levels in plant vasculature. Proc Natl Acad Sci USA 2005, 102(34):12089-12094. 10.1073/pnas.0505927102, 1189354, 16103368.
50. Maeda H, Song W, Sage TL, DellaPenna D. Tocopherols play a crucial role in low-temperature adaptation and Phloem loading in Arabidopsis. Plant Cell 2006, 18(10):2710-2732. 10.1105/tpc.105.039404, 1626601, 17012603.
51. Arenhart RA, Bai Y, de Oliveira LF V, Bucker Neto L, Schunemann M, Maraschin FD, Mariath J, Silverio A, Sachetto-Martins G, Margis R, et al. New insights into aluminum tolerance in rice: the ASR5 protein binds the STAR1 promoter and other aluminum-responsive genes. Mol Plant 2013
52. Herve C, Dabos P, Bardet C, Jauneau A, Auriac MC, Ramboer A, Lacout F, Tremousaygue D. In vivo interference with AtTCP20 function induces severe plant growth alterations and deregulates the expression of many genes important for development. Plant Physiol 2009, 149(3):1462-1477. 10.1104/pp.108.126136, 2649380, 19091878.
53. Welchen E, Gonzalez DH. Differential expression of the Arabidopsis cytochrome c genes Cytc-1 and Cytc-2. Evidence for the involvement of TCP-domain protein-binding elements in anther- and meristem-specific expression of the Cytc-1 gene. Plant Physiol 2005, 139(1):88-100. 10.1104/pp.105.065920, 1203360, 16113211.
54. Zsigmond L, Rigo G, Szarka A, Szekely G, Otvos K, Darula Z, Medzihradszky KF, Koncz C, Koncz Z, Szabados L. Arabidopsis PPR40 connects abiotic stress responses to mitochondrial electron transport. Plant Physiol 2008, 146(4):1721-1737. 10.1104/pp.107.111260, 2287346, 18305213.
55. Krochko JE, Abrams GD, Loewen MK, Abrams SR, Cutler AJ. (+)-Abscisic acid 8'-hydroxylase is a cytochrome P450 monooxygenase. Plant Physiol 1998, 118(3):849-860. 10.1104/pp.118.3.849, 34795, 9808729.
56. Mahony S, Benos PV. STAMP: a web tool for exploring DNA-binding motif similarities. Nucleic Acids Res 2007, 35:W253-258. 10.1093/nar/gkm272, 1933206, 17478497.
57. Kalifa Y, Gilad A, Konrad Z, Zaccai M, Scolnik PA, Bar-Zvi D. The water- and salt-stress-regulated Asr1 (abscisic acid stress ripening) gene encodes a zinc-dependent DNA-binding protein. Biochem J 2004, 381(Pt 2):373-378. 1133842, 15101820.
58. Vignault C, Vachaud M, Cakir B, Glissant D, Dedaldechamp F, Buttner M, Atanassova R, Fleurat-Lessard P, Lemoine R, Delrot S. VvHT1 encodes a monosaccharide transporter expressed in the conducting complex of the grape berry phloem. J Exp Bot 2005, 56(415):1409-1418. 10.1093/jxb/eri142, 15809282.
59. Carrari F, Nunes-Nesi A, Gibon Y, Lytovchenko A, Loureiro ME, Fernie AR. Reduced expression of aconitase results in an enhanced rate of photosynthesis and marked shifts in carbon partitioning in illuminated leaves of wild species tomato. Plant Physiol 2003, 133(3):1322-1335. 10.1104/pp.103.026716, 281627, 14551334.
60. Liu XJ, Prat S, Willmitzer L, Frommer WB. cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class I patatin promoter/GUS-gene fusion. Mol Gen Genet 1990, 223(3):401-406.
61. Ricardi M, Gonzalez R, Iusem N. Protocol: fine-tuning of a Chromatin Immunoprecipitation (ChIP) protocol in tomato. Plant Methods 2010, 6(1):11. 10.1186/1746-4811-6-11, 2859366, 20380723.
62. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10(3):R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
63. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008, 9(9):R137. 10.1186/gb-2008-9-9-r137, 2592715, 18798982.
64. R Development Core Team R: A Language and Environment for Statistical Computing 2011, Vienna, Austria: the R Foundation for Statistical Computing, 3-900051-07-0, Available online at http://www.R-project.org/, R Development Core Team.
65. Livak KJ. ABI Prism 7700 Sequence Detection System 1997, PE Applied Biosystems: Foster City, CA, vol. User Bulletin 2.