Nevershed and inflorescence deficient in abscission are differentially required for cell expansion and cell separation during floral organ abscission in arabidopsis thaliana

Journal of Experimental Botany

Volumn 64, Issue 17, 2013, Pages 5345-5357

  Liu, Bin ^a   Butenko, Melinka A ^b   Shi, Chun Lin ^b   Bolivar, Jenny L ^c   Winge, Per ^a   Stenvik, Grethe Elisabeth ^b   Vie, Ane Kjerst ^a   Leslie, Michelle E ^d   Brembu, Tore ^a   Kristiansen, Wenche ^b   Bones, Atle M ^a   Patterson, Sara E ^c   Liljegren, Sarah J ^e   Aalen, Reidunn B ^b  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

^e UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

ARF GAP; Cell wall degradation; Cell wall loosening; Cell to cell communication; Petal breakstrength; Scanning electron microscopy; Signalling peptide

Indexed keywords

ARABIDOPSIS PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; IDA PROTEIN, ARABIDOPSIS; NEV PROTEIN, ARABIDOPSIS; PEPTIDE;

ARABIDOPSIS; ARF-GAP; ARTICLE; BIOLOGICAL MODEL; CELL PROLIFERATION; CELL WALL; CELL WALL DEGRADATION; CELL WALL LOOSENING; CELL-TO-CELL COMMUNICATION; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HISTOLOGY; INFLORESCENCE; METABOLISM; MUTATION; PETAL BREAKSTRENGTH; PHENOTYPE; PHYSIOLOGY; PROTEIN TRANSPORT; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; SIGNALLING PEPTIDE.; TRANSGENIC PLANT;

ARF-GAP; CELL WALL DEGRADATION; CELL WALL LOOSENING; CELL-TO-CELL COMMUNICATION; PETAL BREAKSTRENGTH; SCANNING ELECTRON MICROSCOPY; SIGNALLING PEPTIDE.;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL PROLIFERATION; CELL WALL; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GTPASE-ACTIVATING PROTEINS; INFLORESCENCE; MODELS, BIOLOGICAL; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEPTIDES; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84891870152     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert232     Document Type: Article

References (52)

1. Aalen RB, Butenko MA, Stenvik GE, Tandstad NM, Patterson SE. 2006. Genetic control of floral abscission. In: de Silva JT, ed. Floriculture, ornamental and plant biotechnology: advances and topical issues . London: Global Science Books, 101-108
2. Aalen RB. 2011. Flower and floral organ abscission - control, gene expression and hormone interaction. In: Yaish MW, ed. The flowering process and its control in plants: gene expression and hormone interaction . Kerala: Research Signpost/Transworld Research Network, 307-327
3. Bleecker AB, Patterson SE. 1997. Last exit: senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9, 1169-1179
4. Bryan A, Racolta A, Tax F, Liljegren SJ. 2012. The social network: receptor kinases and cell fate determination. In: Kemmerling B, Tax F, eds. Receptor-like kinases in plants: from signaling to development . New York, NY: Springer, 41-66
5. Burr CA, Leslie ME, Orlowski SK, Chen I, Wright CE, Daniels MJ, Liljegren SJ. 2011. CAST AWAY, a membrane-associated receptor-like kinase, inhibits organ abscission in Arabidopsis. Plant Physiology 156, 1837-1850
6. Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, Mandal A, Aalen RB. 2003. INFLORESCENCE DEFICIENT IN ABSCISSION controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 15, 2296-2307
7. Butenko MA, Stenvik GE, Alm V, Sæther B, Patterson SE, Aalen RB. 2006. Ethylene dependent and -independent pathways controlling floral abscission are revealed to converge using promoter::reporter gene constructs in the ida abscission mutant. Journal of Experimental Botany 57, 3627-3637
8. Butenko MA, Vie AK, Brembu T, Aalen RB, Bones AM. 2009. Plant peptides in signalling: looking for new partners. Trends in Plant Science 14, 255-263
9. Cai S, Lashbrook CC. 2008. Stamen abscission zone transcriptome profiling reveals new candidates for abscission control: enhanced retention of floral organs in transgenic plants overexpressing Arabidopsis ZINC FINGER PROTEIN2. Plant Physiology 146, 1305- 1321
10. Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL, Zhang S, Walker JC. 2008. Regulation of floral organ abscission in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 105, 15629-15634
11. Clough SJ, Bent AF. 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735-743
12. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139, 5-17
13. Delk NA, Johnson KA, Chowdhury NI, Braam J. 2005. CML24, regulated in expression by diverse stimuli, encodes a potential Ca2+ sensor that functions in responses to abscisic acid, daylength, and ion stress. Plant Physiology 139, 240-253
14. Ecker Jr. 1995. The ethylene signal transduction pathway in plants. Science 268, 667- 675
15. Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW. 2005. AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132, 4563-4574
16. Fernandez DE, Heck GR, Perry SE, Patterson SE, Bleecker AB, Fang SC. 2000. The embryo MADS domain factor AGL15 acts postembryonically: inhibition of perianth senescence and abscission via constitutive expression. Plant Cell 12, 183-198
17. Grini PE, Jürgens G, Hülskamp M. 2002. Embryo and endosperm development is disrupted in the female gametophytic capulet mutants of Arabidopsis. Genetics 162, 1911-1925
18. Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG. 2003. The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 130, 161-172
19. Hepworth SR, Zhang Y, McKim S, Li X, Haughn GW. 2005. BLADE-ON-PETIOLE-dependent signaling controls leaf and floral patterning in Arabidopsis. Plant Cell 17, 1434-1448
20. Kim J, Dotson B, Rey C, Lindsey J, Bleecker AB, Binder BM, Patterson SE. 2013. New Clothes for the jasmonic acid receptor COI1: delayed abscission, meristem arrest, and apical dominance. PLoS ONE 8, e60505
21. Koornneef M, Alonso-Blanco C, Blankestijn-deVries H, Hanhart CJ, Peeters AJM. 1998. Genetic interactions among late-flowering mutants of Arabidopsis. Genetics 148, 885- 892
22. Kumpf RP, Shi CL, Larrieu A, Sto IM, Butenko MA, Peret B, Riiser ES, Bennett MJ, Aalen RB. 2013. Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence. Proceedings of the National Academy of Sciences, USA 110, 5235-5240
23. Kusnierczyk A, Winge P, Midelfart H, Armbruster WS, Rossiter JT, Bones AM. 2007. Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae. Journal of Experimental Botany 58,2537-2552
24. Leslie ME, Lewis MW, Youn JY, Daniels MJ, Liljegren SJ. 2010. The EVERSHED receptor-like kinase modulates floral organ shedding in Arabidopsis. Development 137, 467-476
25. Lewis MW, Leslie ME, Fulcher EH, Darnielle L, Healy PN, Youn JY, Liljegren SJ. 2010. The SERK1 receptor-like kinase regulates organ separation in Arabidopsis flowers. The Plant Journal 62, 817-828
26. Lewis MW, Leslie ME, Liljegren SJ. 2006. Plant separation: 50 ways to leave your mother. Current Opinion in Plant Biology 9, 59-65
27. Liljegren SJ. 2012. Organ abscission: exit strategies require signals and moving traffic. Current Opinion in Plant Biology 15, 670-676
28. Liljegren SJ, Leslie ME, Darnielle L, et al. 2009. Regulation of membrane trafficking and organ separation by the NEVERSHED ARFGAP protein. Development 136, 1909-1918
29. Maris A, Kaewthai N, Eklöf JM, Miller JG, Brumer H, Fry SC, Verbelen JP, Vissenberg K. 2011. Differences in enzymic properties of five recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis thaliana. Journal of Experimental Botany 62, 261-271
30. Maris A, Suslov D, Fry SC, Verbelen JP, Vissenberg K. 2009. Enzymic characterization of two recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis and their effect on root growth and cell wall extension. Journal of Experimental Botany 60, 3959-3972
31. McKim SM, Stenvik GE, Butenko MA, Kristiansen W, Cho SK, Hepworth SR, Aalen RB, Haughn GW. 2008. The BLADEON- PETIOLE genes are essential for abscission zone formation in Arabidopsis. Development 135, 1537-1546
32. Niederhuth C, Patharkar OR, Walker J. 2013. Transcriptional profiling of the Arabidopsis abscission mutant hae hsl2 by RNA-Seq. BMC Genomics 14, 37
33. Obayashi T, Kinoshita K, Nakai K, Shibaoka M, Hayashi S, Saeki M, Shibata D, Saito K, Ohta H. 2007. ATTED-II: A database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Research 35, D863- D869
34. Patterson SE. 2001. Cutting loose. Abscission and dehiscence in Arabidopsis. Plant Physiology 126, 494-500
35. Patterson SE, Bleecker AB. 2004. Ethylene-dependent and -independent processes associated with floral organ abscission in Arabidopsis. Plant Physiology 134, 194-203
36. Patterson SE, Butenko MA, Kim J. 2007. Ethylene responses in abscission and other processes of cell separation in Arabidopsis. In: Ramina A, Chang C, Giovannoni J, Klee H, Parata P, Woltering E, eds. Advances in plant ethylene research . Dordrecht: Springer, 271-278
37. Pfaffl MW, Horgan GW, Dempfle L. 2002. Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30, e36
38. R Development Core Team. 2007. R: A language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria, http://www.R- project.org
39. Rim Y, Jung JH, Chu H, Cho WK, Kim SW, Hong JC, Jackson D, Datla R, Kim JY. 2009. A non-cell-autonomous mechanism for the control of plant architecture and epidermal differentiation involves intercellular trafficking of BREVIPEDICELLUS protein. Functional Plant Biology 36, 280-289
40. Roberts JA, Elliot KA, Gonzalez-Carranza ZH. 2002. Abscission, dehiscence and other cell separation processes. Annual Review of Plant Biology 53, 131-158
41. Schroder F, Lisso J, Lange P, Mussig C. 2009. The extracellular EXO protein mediates cell expansion in Arabidopsis leaves. BMC Plant Biology 9, 20
42. Shi CL, Stenvik GE, Vie AK, Bones AM, Pautot V, Proveniers M, Aalen RB, Butenko MA. 2011. Arabidopsis class I KNOTTEDlike homeobox proteins act downstream in the IDA- HAE/HSL2 floral abscission signaling pathway. Plant Cell 23, 2553-2567
43. Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP. 2007. The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell 19, 2440-2453
44. Singh AP, Tripathi SK, Nath P, Sane AP 2011. Petal abscission in rose is associated with the differential expression of two ethylene-responsive xyloglucan endotransglucosylase/hydrolase genes, RbXTH1 and RbXTH2. Journal of Experimental Botany 62, 5091-5103
45. Smyth GK. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology 3, Article 3
46. Stefano G, Renna L, Rossi M, Azzarello E, Pollastri S, Brandizzi F, Baluska F, Mancuso S. 2010. AGD5 is a GTPase-activating protein at the trans-Golgi network. The Plant Journal 64, 790-799
47. Stenvik GE, Butenko MA, Urbanowicz BR, Rose JK, Aalen RB. 2006. Overexpression of INFLORESCENCE DEFICIENT IN ABSCISSION activates cell separation in vestigial abscission zones in Arabidopsis. Plant Cell 18, 1467-1476
48. Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W, Holmgren A, Clark SE, Aalen RB, Butenko MA. 2008. The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20, 1805-1817
49. Wang XQ, Xu WH, Ma LG, Fu ZM, Deng XW, Li JY, Wang YH. 2006. Requirement of KNAT1/BP for the development of abscission zones in Arabidopsis thaliana. Journal of Integrative Plant Biology 48, 15-26
50. Wilkinson JQ, Lanahan MB, Clark DG, Bleecker AB, Chang C, Meyerowitz EM, Klee HJ. 1997. A dominant mutant receptor fromArabidopsis confers ethylene insensitivity in heterologous plants. Nature Biotechnology 15, 444-447
51. Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW. 2005. NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. The Plant Journal 43, 118-130
52. Xu W, Purugganan MM, Polisensky DH, Antosiewicz DM, Fry SC, Braam J. 1995. Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell 7, 1555-1567