Identification of differentially expressed transcripts for trunk formation in sago palm using annealing control primer GeneFishing technique

Hasnain Hussain Anastasia Shera Edward-Atit Norzainizul Julaihi Rina Tommy Mehvish Nisar Nurhazlina Hamdan Hiroshi Ehara   

Open Access   

Published:  Nov 27, 2021


In the state of Sarawak, Malaysia’s vast peatland cultivated with sago palm (Metroxylon sagu), a considerable amount of cases involving stunted, nondeveloped trunk of sago palms was observed. Molecular-level understanding of the mechanism or pathway involved in the trunking (T) process leading to storage starch accumulation in the trunk of the sago palm is yet to be fully understood. A Polymerase Chain Reaction-based differential display analysis using Annealing Control Primer based GeneFishing technique on leaf samples of normal T compared to the nontrunking (NT) palm showed distinct differentially expressed transcripts pattern with differences in intensity between 35% and 123%. The translated sequence identified functions that are grouped under energy metabolism, nutrient regulation, biosynthetic reactions, defense mechanism, and stress tolerance. Transcripts from T showed higher expression of redox-regulating functions, while NT samples had proteins actively involved in the respiratory chain and chloroplast regulation. In nutrient regulation, the T sample showed higher transcript levels of nitrogen utilization and regulation of phosphate and cobalt, whereas NT showed activities of nitrogen uptake and regulation of calcium, magnesium, and zinc. This study identified different levels of transcripts in two physiologically different sago palms, and the formation and the development of the trunk are induced by these enzymes.

Keyword:     Differential display differentially expressed transcripts (DET) nontrunking trunking sago palm


Hussain H, Edward-Atit AS, Julaihi N, Tommy R, Nisar M, Hamdan N, Ehara H. Identification of differentially expressed transcripts for trunk formation in sago palm using annealing control primer GeneFishing technique. J Appl Biol Biotech. Online First.

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

HTML Full Text


1. Flach M. Sago palm: Metroxylon sagu rottb.-Promoting the conservation and use of underutilized and neglected crops. 13. Bioversity International, Institute of Plant Genetics and Crop Plant Research, Gatersleben, Germany/International Plant Genetic Resources Institute, Rome, Italy, 1997.

2. Lim LWK, Chung HH, Hussain H, Bujang K. Sago palm (Metroxylon sagu Rottb.): now and beyond. Pertanika J Trop Agri Sci 2019;42: 435-51.

3. Achudan SN, Dos Mohamed AM, Abd Rashid RS, Mittis P. Yield and physicochemical properties of starch at different sago palm stages. Mater Today Proc 2020;31:122-6.

4. Ehara H, Toyoda Y, Johnson DV. Sago palm: multiple contributions to food security and sustainable livelihoods. Springer Nature, Basingstoke, UK, 2018.

5. Hussain H, Kamal MM, Al-Obaidi JR, Hamdin NE, Ngaini Z, Mohd- Yusuf Y. Proteomics of sago palm towards identifying contributory proteins in stress-tolerant cultivar. Protein J 2020;39:62-72.

6. Songan P, Noweg GT, Harun WSW, Mohamad M. Sustainable livelihood of peatland dwellers in the Mukah watershed, Sarawak, Malaysia. In International symposium and workshop on tropical peatland, Yogyakarta, Indonesia, pp 171-6, 2007.

7. Apun K, Lihan S, Wong M, Bilung L. Microbiological characteristics of trunking and non-trunking sago palm peat soil: programme and abstract. In 1st ASEAN Sago Symposium 2009: Current Trend and Development in Sago Research, Sarawak, Malaysia, pp 29-30, 2009.

8. Sim S, Wasli M, Yong C, Howell P, Jumin C, Safie N, et al. Assessment of the humification degree of peat soil under sago (Metroxylon sagu) cultivation based on fourier transform infrared (FTIR) and ultraviolet-visible (UV-Vis) spectroscopic characteristics. Mires Peat 2017;19:1-0.

9. Hussain H, Yan WJ, Ngaini Z, Julaihi N, Tommy R, Bhawani SA. Differential metabolites markers from trunking and stressed non-trunking sago palm (Metroxylon sagu Rottb.). Curr Chem Biol 2020;14:262-78.

10. Edward AS, Hussain H. Differential expression gene profiling of trunking and non-trunking sago palm. In: Proceedings of the 2nd Biotechnology Colloquium 2009, Department of Molecular Biology, Faculty of Resource Science and Technology, UNIMAS, Sarawak, Malaysia, 2009.

11. Baena-González E, Sheen J. Convergent energy and stress signaling. Trends Plant Sci 2008;13:474-82.

12. Lim LWK, Chung HH, Hussain H. Complete chloroplast genome sequencing of sago palm (Metroxylon sagu Rottb.): molecular structures, comparative analysis and evolutionary significance. Gene Rep 2020;19:100662.

13. Hwang IT, Kim YJ, Kim SH, Kwak CI, Gu YY, Chun JY. Annealing control primer system for improving specificity of PCR amplification. Biotech 2003;35:1180-4.

14. Schneider CA, Rasband WS, Eliceiri KW. NIH image to ImageJ: 25 years of image analysis. Nat Methods 2012;9:671-5.

15. Thompson JD, Higgins DG, Gibson TJ. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-80.

16. Chen G, Zhang X. New insights into S2P signaling cascades: regulation, variation, and conservation. Protein Sci 2010;19:2015-30.

17. Okamoto S, Yu F, Harada H, Okajima T, Hattan Ji, Misawa N, et al. A short-chain dehydrogenase involved in terpene metabolism from Zingiber zerumbet. FEBS J 2011;278:2892-900.

18. Soberón-Chávez G, Alcaraz LD, Morales E, Ponce-Soto GY, Servín- González L. The transcriptional regulators of the CRP family regulate different essential bacterial functions and can be inherited vertically and horizontally. Front Microbiol 2017;8:959.

19. Kim J, Kwon YS, Bae DW, Kwak YS. Proteomic reference map and comparative analysis between streptomyces griseus S4-7 and wbiE2 transcription factor-mutant strain. Plant Pathol J 2020;36:185.

20. Akbudak MA, Filiz E, Vatansever R, Kontbay K. Genome-wide identification and expression profiling of ascorbate peroxidase (APX) and glutathione peroxidase (GPX) genes under drought stress in Sorghum (Sorghum bicolor L.). J Plant Growth Regul 2018;37: 925-36.

21. Wu B, Wang B. Comparative analysis of ascorbate peroxidases (APXs) from selected plants with a special focus on Oryza sativa employing public databases. PLoS One 2019;14:e0226543.

22. Anjum NA, Gill SS, Gill R, Hasanuzzaman M, Duarte AC, Pereira E, et al. Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple, and associated enzymes. Protoplasma 2014;251:1265- 83.

23. Yang X, Liao CY, Tang J, Bassham DC. Overexpression of trans-Golgi network t-SNARE s rescues vacuolar trafficking and TGN morphology defects in a putative tethering factor mutant. Plant J 2019;99:703-16.

24. Kerscher S, Dröse S, Zickermann V, Brandt U. The three families of respiratory NADH dehydrogenases. Bioenerg 2007;45:185-222.

25. Yamori W, Makino A, Shikanai T. A physiological role of cyclic electron transport around photosystem i in sustaining photosynthesis under fluctuating light in rice. Sci Rep 2016;6:20147.

26. Yamori W, Shikanai T, Makino A. Photosystem i cyclic electron flow via chloroplast nadh dehydrogenase-like complex performs a physiological role for photosynthesis at low light. Sci Rep 2015;5:13908.

27. Strand DD, D'Andrea L, Bock R. The plastid NAD (P) H dehydrogenase-like complex: structure, function and evolutionary dynamics. Biochem J 2019;476:2743-56.

28. González D, Álamos P, Rivero M, Orellana O, Norambuena J, Chávez R, et al. Deciphering the role of multiple thioredoxin fold proteins of Leptospirillum sp. in oxidative stress tolerance. Int J Mol Sci 2020;21:1880.

29. Luan S, Lan W, Lee SC. Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL-CIPK network. Curr Opin Plant Biol 2009;12:339-46.

30. Kim MC, Chung WS, Yun DJ, Cho MJ. Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2009;2:13-21.

31. Taneja M, Tyagi S, Sharma S, Upadhyay SK. Ca2+/cation antiporters (CaCA): identification, characterization and expression profiling in bread wheat (Triticum aestivum L.). Front Plant Sci 2016;7:1775.

32. Chen H, Yue Y, Yu R, Fan Y. A Hedychium coronarium short chain alcohol dehydrogenase is a player in allo-ocimene biosynthesis. Plant Mol Biol 2019;101:297-313.

33. Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, et al. Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Nat Acad Sci 2009;106:3615-20.

34. Yoshida K, Uchikoshi E, Hara S, Hisabori T. Thioredoxin-like2/2- Cys peroxiredoxin redox cascade acts as oxidative activator of glucose-6-phosphate dehydrogenase in chloroplasts. Biochem J 2019;476:1781-90.

35. Kambhampati S, Ajewole E, Marsolais F. Advances in asparagine metabolism. In: Cánovas F, Lüttge U, Matyssek R (eds). Progress in Botany, Springer, Cham, Vietnam, pp 49-74, 2017, vol 79.

36. Gaufichon L, Reisdorf-Cren M, Rothstein SJ, Chardon F, Suzuki A. Biological functions of asparagine synthetase in plants. Plant Sci 2010;179:141-53.

37. Ma Z, Marsolais F, Bykova NV, Igamberdiev AU. Nitric oxide and reactive oxygen species mediate metabolic changes in barley seed embryo during germination. Front Plant Sci 2016;7:138.

38. Berger A, Boscari A, Frendo P, Brouquisse R. Nitric oxide signaling, metabolism and toxicity in nitrogen-fixing symbiosis. J Exp Bot 2019;70:4505-20.

39. Schmitt G, Saft M, Arndt F, Kahnt J, Heider J. Two different quinohemoprotein amine dehydrogenases initiate anaerobic degradation of aromatic amines in Aromatoleum aromaticum EbN1. J Bacteriol 2019;201:e00281-19.

40. Matsumoto M, Osaki M, Nuyim T, Jongskul A, Eam-on P, Kitaya Y, et al. Nutritional characteristics of sago palm and oil palm in tropical peat soil. J Plant Nutr 1998;21:1819-41.

41. Moreau P, Brandizzi F, Hanton S, Chatre L, Melser S, Hawes C, et al. The plant ER-Golgi interface: a highly structured and dynamic membrane complex. J Exp Bot 2007;58:49-64.

42. Phan NQ, Kim SJ, Bassham DC. Overexpression of Arabidopsis sorting nexin AtSNX2b inhibits endocytic trafficking to the vacuole. Mol Plant 2008;1:961-76.

43. Brumbarova T, Ivanov R. Differential gene expression and protein phosphorylation as factors regulating the state of the Arabidopsis SNX1 protein complexes in response to environmental stimuli. Front Plant Sci 2016;7:1456.

44. Jaillais Y, Fobis-Loisy I, Miège C, Gaude T. Evidence for a sorting endosome in Arabidopsis root cells. Plant J 2008;53:237-47.

45. Calderón A, Sevilla F, Jiménez A. Redox protein thioredoxins: function under salinity, drought and extreme temperature conditions. In: Gupta D, Palma J, Corpas F (eds). Antioxidants and Antioxidant Enzymes in Higher Plants, Springer, New York, NY, pp 123-62, 2018.

46. Ning P, Yang L, Li C, Fritschi FB. Post-silking carbon partitioning under nitrogen deficiency revealed sink limitation of grain yield in maize. J Exp Bot 2018;69:1707-19.

47. Lane TS, Rempe CS, Davitt J, Staton ME, Peng Y, Soltis DE, et al. Diversity of ABC transporter genes across the plant kingdom and their potential utility in biotechnology. BMC Biotechnol 2016;16:1-0.

48. Zhou P, Pu T, Gui C, Zhang X, Gong L. Transcriptome analysis reveals biosynthesis of important bioactive constituents and mechanism of stem formation of Dendrobium huoshanense. Scie Rep 2020;10:1-1.

49. Liu F, Chang XJ, Ye Y, Xie WB, Wu P, Lian XM. Comprehensive sequence and whole-life-cycle expression profile analysis of the phosphate transporter gene family in rice. Mol Plant 2011;4:1105-22.

50. Bao Z, Qi X, Hong S, Xu K, He F, Zhang M, et al. Structure and mechanism of a group-I cobalt energy coupling factor transporter. Cell Res 2017;27:675-87.

51. Akeel A, Jahan A. Role of cobalt in plants: its stress and alleviation. In: Naeem M, Ansari A, Gill S (eds). Contaminants in Agriculture, Springer, New York, NY, pp 339-57, 2020.

52. Erbs G, Molinaro A, Dow J, Newman MA. Lipopolysaccharides and plant innate immunity. In: Wang X, Quinn P (eds). Endotoxins: Structure, Function and Recognition, Springer, New York, NY, pp 387-403, 2010.

53. Sato N, Takano H. Diverse origins of enzymes involved in the biosynthesis of chloroplast peptidoglycan. J Plant Res 2017;130:635-45.

55. Ukleja M, Valpuesta JM, Dziembowski A, Cuellar J. Beyond the known functions of the CCR4-NOT complex in gene expression regulatory mechanisms: new structural insights to unravel CCR4- NOT mRNA processing machinery. Bioessays 2016;38:1048-58.

54. Lin X, Li N, Kudo H, Zhang Z, Li J, Wang L, et al. Genes sufficient for synthesizing peptidoglycan are retained in gymnosperm genomes, and MurE from Larix gmelinii can rescue the albino phenotype of Arabidopsis MurE mutation. Plant Cell Physiol 2017;58:587-97.

56. Singhania RR, Patel AK, Pandey A, Ganansounou E. Genetic modification: a tool for enhancing beta-glucosidase production for biofuel application. Bioresour Technol 2017;245:1352-61.

57. Morant AV, Jørgensen K, Jørgensen C, Paquette SM, Sánchez-Pérez R, Møller BL, et al. β-Glucosidases as detonators of plant chemical defense. Phytochem 2008;69:1795-813.

58. Andrási N, Rigó G, Zsigmond L, Pérez-Salamó I, Papdi C, Klement E, et al. The mitogen-activated protein kinase 4-phosphorylated heat shock factor A4A regulates responses to combined salt and heat stresses. J Exp Bot 2019;70:4903-18.

59. Adamiec M, Ciesielska M, Zala? P, Luci?ski R. Arabidopsis thaliana intramembrane proteases. Acta Physiol Plant 2017;39:1-7.

60. Kinch LN, Ginalski K, Grishin NV. Site-2 protease regulated intramembrane proteolysis: sequence homologs suggest an ancient signaling cascade. Protein Sci 2006;15:84-93.

61. Hsieh EJ, Waters BM. Alkaline stress and iron deficiency regulate iron uptake and riboflavin synthesis gene expression differently in root and leaf tissue: implications for iron deficiency chlorosis. J Exp Bot 2016;67:5671-85.

62. Roje S. Vitamin B biosynthesis in plants. Phytochem 2007;68:1904-21.

63. Hohmann S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 2002;66:300-72.

64. Singh V, Singh PK, Siddiqui A, Singh S, Banday ZZ, Nandi AK. Over-expression of Arabidopsis thaliana SFD1/GLY1, the gene encoding plastid localized glycerol-3-phosphate dehydrogenase, increases plastidic lipid content in transgenic rice plants. J Plant Res 2016;129:285-93.

65. Zhao Y, Li X, Wang F, Zhao X, Gao Y, Zhao C, et al. Glycerol-3- phosphate dehydrogenase (GPDH) gene family in Zea mays L.: identification, subcellular localization, and transcriptional responses to abiotic stresses. PloS One 2018;13:e0200357.

66. Saier Jr MH. The bacterial phosphotransferase system: new frontiers 50 years after its discovery. J Mol Microbiol Biotechnol 2015;25:73-8.

67. Zheng T, Zang L, Dai L, Yang C, Qu G. Two novel eukaryotic translation initiation factor 5A genes from Populus simonii × P. nigra confer tolerance to abiotic stresses in Saccharomyces cerevisiae. J For Res 2017;28:453-63.

68. Taw MN, Lee HI, Lee SH, Chang WS. Characterization of MocR, a GntR-like transcriptional regulator, in Bradyrhizobium japonicum: its impact on motility, biofilm formation, and soybean nodulation. J Microbiol 2015;53:518-25.

69. Wang TW, Lu L, Wang D, Thompson JE. Isolation and characterization of senescence-induced cDNAs encoding deoxyhypusine synthase and eucaryotic translation initiation factor 5A from tomato. J Biol Chem 2001;276:17541-9.

70. Thompson JE, Hopkins MT, Taylor C, Wang TW. Regulation of senescence by eukaryotic translation initiation factor 5A: implications for plant growth and development. Trends Plant Sci 2004;9:174-9.

71. Rigali S, Derouaux A, Giannotta F, Dusart J. Subdivision of the helix-turn-helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J Biol Chem 2002;277:12507-15.

72. Geddes BA, Paramasivan P, Joffrin A, Thompson AL, Christensen K, Jorrin B, et al. Engineering transkingdom signalling in plants to control gene expression in rhizosphere bacteria. Nature Commun 2019;10:1-1.

73. Magarvey N, He J, Aidoo K, Vining L. The pdx genetic marker adjacent to the chloramphenicol biosynthesis gene cluster in Streptomyces venezuelae ISP5230: functional characterization The GenBank accession number for the sequence reported in this paper is AF286159. Microbiol 2001;147:2103-12.

74. Nonaka S, Someya T, Zhou S, Takayama M, Nakamura K, Ezura H. An Agrobacterium tumefaciens strain with gamma-aminobutyric acid transaminase activity shows an enhanced genetic transformation ability in plants. Sci Rep 2017;7:1-1.

Article Metrics

1 Absract views 0 PDF Downloads 1 Total views

Related Search

By author names

    Warning: Cannot modify header information - headers already sent by (output started at /home/jabonlin/public_html/jab_php/abstract.php:235) in /home/jabonlin/public_html/jab_php/articlemodule/searchArticles.php on line 1162

    Warning: Invalid argument supplied for foreach() in /home/jabonlin/public_html/jab_php/abstract.php on line 819

Citiaion Alert By Google Scholar

Name Required
Email Required Invalid Email Address

Comment required

Notice: Undefined variable: dbq35 in /home/jabonlin/public_html/jab_php/abstract.php on line 942

Warning: mysqli_num_rows() expects parameter 1 to be mysqli_result, null given in /home/jabonlin/public_html/jab_php/articlemodule/database.php on line 379
Similar Articles