Insights into transcriptional regulation of β-D-N-acetylhexosaminidase, an N-glycan-processing enzyme involved in ripening-associated fruit softening

Journal of Experimental Botany

Volumn 65, Issue 20, 2014, Pages 5835-5848

  Irfan, Mohammad ^a   Ghosh, Sumit ^a,b   Kumar, Vinay ^a   Chakraborty, Niranjan ^a   Chakraborty, Subhra ^a   Datta, Asis ^a  

^a NATIONAL INSTITUTE OF PLANT GENOME RESEARCH   (India)

^b CSIR CENTRAL INSTITUTE OF MEDICINAL AND AROMATIC PLANTS   (India)

Author keywords

Fruit ripening; fruit ripening specific promoter; RIN; SlASR1; transcriptional regulation; Hex

Indexed keywords

ABSCISIC ACID; BETA N ACETYLHEXOSAMINIDASE; ETHYLENE DERIVATIVE; GLUCAN; MADS DOMAIN PROTEIN; PHYTOHORMONE; VEGETABLE PROTEIN;

ENZYMOLOGY; FLOWER; FRUIT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PLANT LEAF; PLANT ROOT; PLANT STEM; PROMOTER REGION; TOMATO; TWO HYBRID SYSTEM;

ABSCISIC ACID; BETA-N-ACETYLHEXOSAMINIDASES; ETHYLENES; FLOWERS; FRUIT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GLUCANS; LYCOPERSICON ESCULENTUM; MADS DOMAIN PROTEINS; PLANT GROWTH REGULATORS; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PLANT STEMS; PROMOTER REGIONS, GENETIC; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84913529754     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru324     Document Type: Article

References (55)

1. Amitai-Zeigerson H, Scolnik PA, Bar-Zvi D. 1995. Tomato Asr1 mRNA and protein are transiently expressed following salt stress, osmotic stress and treatment with abscisic acid. Plant Science 110, 205-213.
2. Bovy A de Vos R Kemper M et al. 2002 High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor gene LC and C1 The Plant Cell 14 2509-2526
3. Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R. 2003. A grape ASR protein involved in sugar and abscisic acid signaling. The Plant Cell 15, 2165-218 0.
4. Cao L, Zhao C, Su S, Luo C, Han M. 2014. The role of fi-hexosaminidase in peach (Prunus persica) fruit softening. Scientia Horticulturae 169, 226-233.
5. Cartharius K, Frech K, G rote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T. 2005. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21, 2933-2942.
6. Dong T, Chen G, Tian S, Xie Q, Yin W, Zhang Y, Hu Z. 2014. A nonclimacteric fruit gene CaMADS-RIN regulates fruit ripening and ethylene biosynthesis in climacteric fruit. PLoS One 9, e95559.
7. Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19, 11-15.
8. Fillati JJ, Kiser J, Rose R, Comai L. 1987. Efficient transfer of a C glyphosphate tolerance gene into tomato using a binary Agrobacterium tumifaciens vector. Biotechnology 5, 726-730.
9. Fujisawa M, Nakano T, Ito Y. 2011. Identification of potential target genes for the tomato fruit-ripening regulator RIN by chromatin immunoprecipitation. BMC Plant Biology 11, 26-40.
10. Fujisawa M, Nakano T, Shima Y, Ito Y. 2013. A large-scale identification of direct targ ets of the tomato MADS Box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. The Plant Cell 25, 371-386.
11. Fujisawa M, Shima Y, Higuchi N, Nakano T, Koyama Y, Kasumi T, Ito Y . 2012. Direct targets of the tomato-ripening regulator RIN identified by transcriptome and chromatin immunoprecipitation analyses. Planta 235, 1107-1122.
12. Ghosh S, Meli VS, Kumar A, Thakur A, Chakrabort y N, Chakraborty S, Datta A. 2011. The N-glycan processing enzymes fi-mannosidase and fi-D-N-acetylhexosaminidase are involved in ripening-associated softening in the nonclimacteric fruits of capsicum. Journal of Experimental Botany 62, 571-582.
13. Ghosh S, Singh UK, Meli VS, Kumar V, Kumar A, Irfan M, Chakraborty N, Chakraborty S, Datta A. 2013. Induction of senescence and identification of differentially expressed genes i n tomato in response to monoterpene. PLoS One 8, e76029.
14. Giovannoni JJ. 2007. Fruit ripening mutants yield insights into ripening control. Current Opinion in Plant Biology 10, 283-289.
15. G utternigg M, Kretschmer-Lubich D, Paschinger K, Rendifi D, Hader J, Geier P, Ranftl R, Jantsch V, Lochnit G, Wilson IB. 2007. Biosynthesis of truncated N-linked oligosaccharides results from non-orthologous hex osaminidase-mediated mechanisms in nematodes, plants, and insects. Journal of Biological Chemistry 282, 27825-27840.
16. Handa AK, Singh NK, Biggs SM. 1985. Effect of tunicamycin on in vitro ripening of tomato pericarp tissue. Plant Physiology 63, 417-424.
17. Higo K, Ugawa Y, Iwamoto M, Korenaga T. 1999. Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Research 27, 297-300.
18. Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, Yasuda J, Ito H, Inakuma T, Hiroi S, Kasumi T. 2008. DNA-binding specificity, transcriptional activation potential, and the rin mutation effect f or the tomato fruit-ripening regulator RIN. The Plant Journal 55, 212-223.
19. Iusem ND, Bartholomew DM, Hitz WD, Scolnik PA. 1993. Tomato (Lycopersicon esculentum) transcript induced by water deficit and ripening. Plant Physiology 102, 1353-1354.
20. Jagadeesh BH, Prabha TN. 2002. fi-Hexosaminidase, an enzyme from ripening bell capsicum (Capsicum annuum var. variata). Phytochemistry 61, 295-300.
21. Jagadeesh BH, Prabha TN, Srinivasan K. 20 04. Activities of glycosidases during fruit development and ripening of tomato (Lycopersicon esculentum L.): Implication in fruit ripening. Plant Science 166, 1451-1459.
22. Jefferson RA, Kavanagh TA, Bevan MW. 1987. GUS fusions: fi-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. The EMBO Journal 6, 3901-3907.
23. Kalifa Y, Gilad A, Konrad Z, Zaccai M, Scolnik PA, Bar-Zvi D. 2004a . The water-and salt-stress-regulated Asr1 (abscisic acid stress ripening) gene encodes a zinc-dependent DNA-binding protein. Biochemical Journal 381, 373-378.
24. Kalifa Y Perlson E Gilad A Konrad Z Scolnik PA Bar-Zvi D. 2004 Over-expression of the water and salt stress-regulated Asr1 gene confers an increased salt tolerance Plant, Cell and Environment 27 1459-1468.
25. Kim S, Park M, Yeom SI et al. 2014. Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nature Genetics 46, 270-278.
26. Klee HJ, Giovannoni JJ. 2011. Genetics and control of tomato fruit ripening and quality attributes. Annual Review of Genetics 45, 41-59.
27. Kumar R, Sharma MK, Kapoor S, Tyagi AK, Sharma AK. 2012. Transcriptome analysis of rin mutant fruit and in silico anal ysis of promoters of differentially regulated genes provides insight into LeMADS-RINregulated ethylene-dependent as well as ethylene-independent aspects of ripening in tomato. Molecular Genetics and Genomics 287, 189-203.
28. Lee S, Chung EJ, Joung YH, Choi D. 2010. Non-climacteric fruit ripening in pepper: increased transcription of EIL-like genes normally regulated by ethylene. Functional and Integrative Genomics 10, 135-146.
29. Lescot M, Déhais P, Moreau Y, De Moor B, Rouzé P, Rombauts. 2002. PlantCARE: a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30, 325-327.
30. Liebminger E, Veit C, Pabst M, Batoux M, Zipfel C, Altmann F, Mach L, Strasser R. 2011. fi-N-Acetylhexosaminidases HEXO1 and HEXO3 are responsible for the formation of paucimannosidic N-glycans i n Arabidopsis thaliana. Journal of Biological Chemistry 286, 10793-10802.
31. Liu Y, Schiff M, Dinesh-Kumar SP. 2002. Virus-induced gene silencing in tomato. The Plant Journal 31, 777-786.
32. Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ. 2011. The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent man ner. Plant Physiology 157, 1568-1579.
33. Meli VS, Ghosh S, Prabha TN, Chakraborty N, Chakraborty S, Datta A. 2010. Enhancement of fruit shelf life by suppressing N-glycan processing enzymes. Proceedings of the National Academy of Sciences, USA 107, 2413-2418.
34. Menke FLH, Parchmann S, Mueller MJ, Kijne JW, Memelink J. 1999. Involvement of the octadecanoid pathway and protein phosphorylation in fungal elicitor-induced expression of terpenoid indole alkaloid biosynthesis genes in C atharanthus roseus. Plant Physiology 119, 1289-1296.
35. Orzaez DF, Mirabel S, Wieland WH, Granell A. 2006. Agroinjection of tomato fruits, a tool for rapid functional analysis of transgenes directly in pla nt. Plant Physiology 140, 3-11.
36. Osorio S, Alba R, Nikoloski Z, Kochevenko A, Fernie AR, Giovannoni JJ. 2012. Integrative comparative analyses of transcript and metabolite profiles from pepper a nd tomato ripening and development stages uncovers species-specific patterns of network regulatory behavior. Plant Physiology 159, 1713-1729.
37. Osorio S, Scossa F, Fernie AR. 2013. Molecular regulation of fruit ripening. Frontiers in Plant Science 4, 198. doi:10.3389/fpls.2013.00198.
38. Priem B, Gitti R, Bush CA, Gross KC. 1993. Structure of ten free N-glycans in ripening tomato fruit (arabinose is a constituent o f a plant N-glycan). Plant Physiology 102, 445-458.
39. Priem B, Gross KC. 1992. Mannosyl-and xylosyl-containing glycans promote tomato (Lycopersicon esculentum Mill.) fruit ripening. Plant Physiology 98, 399-401.
40. Qin G, Wang Y, Cao B, Wang W, Tian S. 2012. Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. The Plant Journal 70, 243-255.
41. Ricardi MM, Gonzale RM, Zhong S et al. 2014. 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 14, 29.
42. Ricardi MM, Guaimas FF, Gonz ález RM, Burrieza HP, López-Fernández MP, Jares-Erijman EA, Esté vez JM, Iusem ND. 2012. Nuclear import and dimerization of tomato ASR1, a water stress-inducible protein exclusive to plants. PLoS One 7, e41008.
43. Rice P, Longden I, Bleasby A. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends in Genetics 16, 276-277.
44. Seymour GB, Chapman NH, Chew BL, Rose JKC. 2013a. Regulation of ripening and opportunities for control in tomato and other fruits. Plant Biotechnology Journal 11, 269-278.
45. Seymour GB, stergaard L, Chapman NH, Knapp S, Martin C. 2013b. Fruit development and ripening. Annual Review of Plant Biology 64 219-241.
46. Shkolnik D, Bar-Zvi D. 2008. Tomato ASR1 abrogates the response to abscisic acid and glucose in Arab idopsis by competing with ABI4 for DNA binding. Plant Biotechnology Journal 6, 368-378.
47. Slamova K, Bojarova P, Petraskova L, Kren V. 2010. fi-NAcetylhexosaminidase: What?s in a name?fi Biotechnology Advances 28, 682-693.
48. Strasser R, Bondili JS, Schoberer J, Svoboda B, Liebminger E, Glössl J, Altmann F, Steinkellner H, Mach L. 2007 . Enzymatic properties and subcellular localization of Arabidopsis fi-Nacetylhexosaminidases. Plant Physiology 145, 5-16.
49. Sun L, Sun Y, Zhang M et al. 2012. Suppression of 9-cisepoxycarotenoid dioxygen ase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiology 158, 283-298.
50. Sun L, Wang YP, Chen P, Ren J, Ji K, Li Q, Li P, Dai SJ, Leng P. 2011. Transcriptional regulation of SlPYL, SlPP2C, and SlSnRK2 gene families encoding ABA signal core components during tomato fruit development and drought stress. Journal of Experimental Botany 62, 5659-5669.
51. Tigchelaar EC, McGlasson WB, Buescher RW. 1978. Genetic regulation of tomato fruit ripening. HortScience 13, 508-513.
52. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J. 2002. A MADS-Box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) Locus. Science 296, 343-346.
53. Wilkinson JQ, Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ. 1995. An ethylene-inducible component of signal transduction encoded by never-ripe. Science 270, 1807-1809.
54. Zhang M, Yuan B, Leng P. 2009. The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. Journal of Experimental Botany 60, 1579-1588.
55. Zhong S, Fei Z, Chen YR et al. 2013. Single-base resolution methylomes of tomato fruit development reveal epig enome modifications associated with ripening. Nature Biotechnology 31, 154-159.