Genome-wide identification and expression analysis of the β-amylase genes strongly associated with fruit development, ripening, and abiotic stress response in two banana cultivars

Hongxia MIAO, Peiguang SUN, Yulu MIAO, Juhua LIU, Jianbin ZHANG, Caihong JIA, Jingyi WANG, Zhuo WANG, Zhiqiang JIN, Biyu XU

PDF(1111 KB)
PDF(1111 KB)
Front. Agr. Sci. Eng. ›› 2016, Vol. 3 ›› Issue (4) : 346-356. DOI: 10.15302/J-FASE-2016127
RESEARCH ARTICLE
RESEARCH ARTICLE

Genome-wide identification and expression analysis of the β-amylase genes strongly associated with fruit development, ripening, and abiotic stress response in two banana cultivars

Author information +
History +

Abstract

β-amylase (BAM) is an important enzyme involved in conversion of starch to maltose in multiple biological processes in plants. However, there is currently insufficient information on the BAM gene family in the important fruit crop banana. This study identified 16 BAM genes in the banana genome. Phylogenetic analysis showed that MaBAMs were classified into four subfamilies. Most MaBAMs in each subfamily shared similar gene structures. Conserved motif analysis showed that all identified MaBAM proteins had the typical glyco hydro 14 domains. Comprehensive transcriptomic analysis of two banana genotypes revealed the expression patterns of MaBAMs in different tissues, at various stages of fruit development and ripening, and in responses to abiotic stresses. Most MaBAMs showed strong transcript accumulation changes during fruit development and late-stage ripening. Some MaBAMs showed significant changes under cold, salt, and osmotic stresses. This finding indicated that MaBAMs might be involved in regulating fruit development, ripening, and responses to abiotic stress. Analysis of five hormone-related and seven stress-relevant elements in the promoters of MaBAMs further revealed that BAMs participated in various biological processes. This systemic analysis provides new insights into the transcriptional characteristics of the BAM genes in banana and may serve as a basis for further functional studies of such genes.

Keywords

β-amylase / banana / genome-wide identification / fruit development / abiotic stress

Cite this article

Download citation ▾
Hongxia MIAO, Peiguang SUN, Yulu MIAO, Juhua LIU, Jianbin ZHANG, Caihong JIA, Jingyi WANG, Zhuo WANG, Zhiqiang JIN, Biyu XU. Genome-wide identification and expression analysis of the β-amylase genes strongly associated with fruit development, ripening, and abiotic stress response in two banana cultivars. Front. Agr. Sci. Eng., 2016, 3(4): 346‒356 https://doi.org/10.15302/J-FASE-2016127

References

[1]
Sethi S, Saini J S, Mohan A, Brar N K, Verma S, Sarao N K, Gill K S. Comparative and evolutionary analysis of α-amylase gene across monocots and dicots. Functional & Integrative Genomics, 2016, 16(5): 545–555
CrossRef Google scholar
[2]
Zanella M, Borghi G L, Pirone C, Thalmann M, Pazmino D, Costa A, Santelia D, Trost P, Sparla F. β-amylase 1 (BAM1) degrades transitory starch to sustain proline biosynthesis during drought stress. Journal of Experimental Botany, 2016, 67(6): 1819–1826
CrossRef Google scholar
[3]
Smith A M, Zeeman S C, Smith S M. Starch degradation. Annual Review of Plant Biology, 2005, 56: 73–98
CrossRef Google scholar
[4]
Zeeman S C, Delatte T, Messerli G, Umhang M, Stettler M, Mettler T, Streb S, Reinhold H, Kotting O. Starch breakdown: recent discoveries suggest distinct pathways and novel mechanisms. Functional Plant Biology, 2007, 34(6): 465–473
CrossRef Google scholar
[5]
Valerio C, Costa A, Marri L, Issakidis-Bourguet E, Pupillo P, Trost P, Sparla F. Thioredoxin-regulated β-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. Journal of Experimental Botany, 2011, 62(2): 545–555
CrossRef Google scholar
[6]
Asatsuma S, Sawada C, Itoh K, Okito M, Kitajima A, Mitsui T. Involvement of α-amylase I-1 in starch degradation in rice chloroplasts. Plant & Cell Physiology, 2005, 46(6): 858–869
CrossRef Google scholar
[7]
Ziegler P. Cereal β-amylases. Journal of Cereal Science, 1999, 29(3): 195–204
CrossRef Google scholar
[8]
Weise S E, Weber A P, Sharkey T D. Maltose is the major form of carbon exported from the chloroplast at night. Planta, 2004, 218(3): 474–482
CrossRef Google scholar
[9]
Vester-Christensen M B, Hachem M A, Svensson B, Henriksen A. Crystal structure of an essential enzyme in seed starch degradation: barley limit dextrinase in complex with cyclodextrins. Journal of Molecular Biology, 2010, 403(5): 739–750
CrossRef Google scholar
[10]
Sørensen A, Ahring B K, Lübeck M, Ubhayasekera W, Bruno K S, Culley D E, Lübeck P S. Identifying and characterizing the most significant β-glucosidase of the novel species Aspergillus. Canadian Journal of Microbiology, 2012, 58(9): 1035–1046
CrossRef Google scholar
[11]
Mizanur R M, Griffin A K, Pohl N L. Recombinant production and biochemical characterization of a hyperthermostable α-glucan/maltodextrin phosphorylase from Pyrococcus furiosus. Archaea, 2008, 2(3): 169–176
CrossRef Google scholar
[12]
Lloyd J R, Kossmann J, Ritte G. Leaf starch degradation comes out of the shadows. Trends in Plant Science, 2005, 10(3): 130–137
CrossRef Google scholar
[13]
Yu T S, Zeeman S C, Thorneycroft D, Fulton D C, Dunstan H, Lue W L, Hegemann B, Tung S Y, Umemoto T, Chapple A, Tsai D L, Wang S M, Smith A M, Chen J, Smith S M. α-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. Journal of Biological Chemistry, 2005, 280(11): 9773–9779
CrossRef Google scholar
[14]
Fulton D C, Stettler M, Mettler T, Vaughan C K, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, Dorken G, Halliday K, Smith A M, Smith S M, Zeeman S C. β-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell, 2008, 20(4): 1040–1058
CrossRef Google scholar
[15]
Srivastava G, Kayastha A M. β-Amylase form starchless seeds of trigonella foenum-graecum and its localization in germinating seeds. PLoS One, 2014, 9(2): e88697
CrossRef Google scholar
[16]
Mason-Gamer R J. The β-amylase genes of grasses and a phylogenetic analysis of the Triticeae (Poaceae). American Journal of Botany, 2005, 92(6): 1045–1058
CrossRef Google scholar
[17]
Reinhold H, Soyk S, Simkova K, Hostettler C, Marafino J, Mainiero S, Vaughan C K, Monroe J D, Zeeman S C. β-amylase-like proteins function as transcription factors in Arabidopsis, controlling shoot growth and development. Plant Cell, 2011, 23(4): 1391–1403
CrossRef Google scholar
[18]
Vinje M A, Willis D K, Duke S H, Henson C A. Differential expression of two β-amylase genes (Bmy1 and Bmy2) in developing and mature barley grain. Planta, 2011, 233(5): 1001–1010
CrossRef Google scholar
[19]
Francisco P, Li J, Smith S M. The gene encoding the catalytically inactive β-amylase BAM4 involved in starch breakdown in Arabidopsis leaves is expressed preferentially in vascular tissues in source and sink organs. Journal of Plant Physiology, 2010, 167(11): 890–895
CrossRef Google scholar
[20]
Prasch C M, Ott K V, Bauer H, Ache P, Hedrich R, Sonnewald U. β-amlyase 1 mutant Arabidopsis plants show improved drought tolerance due to reduced starch breakdown in guard cells. Journal of Experimental Botany, 2015, 66(19): 6059–6067
CrossRef Google scholar
[21]
Monroe J D, Storm A R, Badley E M, Lehman M D, Platt S M, Saunders L K, Schmitz J M, Torres C E. β-amylase1 and β-amylase3 are plastidic starch hydrolases in Arabidopsis that seem to be adapted for different thermal, pH, and stress conditions. Plant Physiology, 2014, 166(4): 1748–1763
CrossRef Google scholar
[22]
Kaplan F, Guy C L. RNA interference of Arabidopsis β-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant Journal, 2005, 44(5): 730–743
CrossRef Google scholar
[23]
Ahmed I M, Cao F, Han Y, Nadira U A, Zhang G, Wu F. Differential changes in grain ultrastructure, amylase, protein and amino acid profiles between Tibetan wild and cultivated barleys under drought and salinity alone and combined stress. Food Chemistry, 2013, 141(3): 2743–2750
CrossRef Google scholar
[24]
Bierhals J D, Lajolo F M, Cordenunsi B R, Oliveira do Nascimento J R. Activity, cloning, and expression of an isoamylase-type starch-debranching enzyme from banana fruit. Journal of Agricultural and Food Chemistry, 2004, 52(24): 7412–7418
CrossRef Google scholar
[25]
D’Hont A, Denoeud F, Aury J M, Baurens F C, Carreel F, Garsmeur O, Noel B, Bocs S, Droc G, Rouard M, Da Silva C, Jabbari K, Cardi C, Poulain J, Souquet M, Labadie K, Jourda C, Lengellé J, Rodier-Goud M, Alberti A, Bernard M, Correa M, Ayyampalayam S, Mckain M R, Leebens-Mack J, Burgess D, Freeling M, Mbéguié-A-Mbéguié D, Chabannes M, Wicker T, Panaud O, Barbosa J, Hribova E, Heslop-Harrison P, Habas R, Rivallan R, Francois P, Poiron C, Kilian A, Burthia D, Jenny C, Bakry F, Brown S, Guignon V, Kema G, Dita M, Waalwijk C, Joseph S, Dievart A, Jaillon O, Leclercq J, Argout X, Lyons E, Almeida A,Jeridi M, Dolezel J, Roux N, Risterucci A M, Weissenbach J, Ruiz M, Glaszmann J C, Quétier F, Yahiaoui N, Wincker P. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature, 2012, 488(7410): 213–217
[26]
Ravi I, Uma S, Vaganan M M, Mustaffa M M. Phenotyping bananas for drought resistance. Frontiers in Physiology, 2013, 4(4): 9
[27]
Yan Y, Takáč T, Li X, Chen H, Wang Y, Xu E, Xie L, Su Z, Šamaj J, Xu C. Variable content and distribution of arabinogalactan proteins in banana (Musa spp.) under low temperature stress. Frontiers in Plant Science, 2004, 6: 353
[28]
Yang Q S, Gao J, He W D, Dou T X, Ding I J, Wu J H, Li C Y, Peng X X, Zhang S, Yi G J. Comparative transcriptomics analysis reveals difference of key gene expression between banana and plantain in response to cold stress. BMC Genomics, 2015, 16(1): 446
CrossRef Google scholar
[29]
Hirayama T, Shinozaki K. Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant Journal, 2010, 61(6): 1041–1052
CrossRef Google scholar
[30]
Hu W, Wang L, Tie W, Yan Y, Ding Z, Liu J, Li M, Peng M, Xu B, Jin Z. Genome-wide analyses of the bZIP family reveal their involvement in the development, ripening and abiotic stress response in banana. Scientific Reports, 2016, 6: 30203
CrossRef Google scholar
[31]
do Nascimento J R O, Júnior A V, Bassinello P Z, Cordenunsi B R, Mainardi J A, Purgatto E, Lajolo F M. β-amylase expression and starch degradation during banana ripening. Postharvest Biology and Technology, 2006, 40(1): 41–47
CrossRef Google scholar
[32]
Pua E C, Chandramouli S, Han P, Liu P. Malate synthase gene expression during fruit ripening of Cavendish banana (Musa acuminata cv. Williams). Journal of Experimental Botany, 2003, 54(381): 309–316
CrossRef Google scholar
[33]
Finn R D, Clements J, Eddy S R. HMMER web server: interactive sequence similarity searching. Nucleic Acids Research, 2011, 39(suppl): 29–37
CrossRef Google scholar
[34]
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 2011, 28(10): 2731–2739
CrossRef Google scholar
[35]
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley D R, Pimentel H, Salzberg S L, Rinn J L, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols, 2012, 7(3): 562–578
CrossRef Google scholar
[36]
Peng T, Zhu X, Duan N, Liu J H. PtrBAM1, a β-amylase-coding gene of Poncirus trifoliata, is a CBF regulon member with function in cold tolerance by modulating soluble sugar levels. Plant, Cell & Environment, 2014, 37(12): 2754–2767
CrossRef Google scholar
[37]
Yoshigi N, Okada Y, Sahara H, Tamaki T. A structural gene encoding β-amylase of barley. Bioscience, Biotechnology, and Biochemistry, 1995, 59(10): 1991–1993
CrossRef Google scholar
[38]
Rajapakse S, Nilmalgoda S D, Molnar M, Ballard R E, Austin D F, Bohac J R. Phylogenetic relationships of the sweetpotato in Ipomoea series Batatas (Convolvulaceae) based on nuclear β-amylase gene sequences. Molecular Phylogenetics and Evolution, 2004, 30(3): 623–632
CrossRef Google scholar
[39]
Zhang D, Wang Y. β-amylase in developing apple fruits: activities, amounts and subcellular localization. Science China. Life Sciences, 2002, 45(4): 429–440
CrossRef Google scholar
[40]
Rorat T, Sadowski J, Irzykowski W, Ziegler P, Daussant J. Differential expression of two β-amylase genes of rye during seed development. Physiologia Plantarum, 1995, 94(1): 19–24
CrossRef Google scholar
[41]
Shiga T M, Soares C A, Nascimento J R, Purgatto E, Lajolo F M, Cordenunsi B R. Ripening-associated changes in the amounts of starch and non-starch polysaccharides and their contributions to fruit softening in three banana cultivars. Journal of the Science of Food and Agriculture, 2011, 91(8): 1511–1516
CrossRef Google scholar
[42]
Etienne A, Génard M, Bugaud C. A process-based model of TCA cycle functioning to analyze citrate accumulation in pre- and post-harvest fruits. PLoS One, 2015, 10(6): e0126777
CrossRef Google scholar
[43]
Maria T, Tsaniklidis G, Delis C, Nikolopoulou A E, Nikoloudakis N, Karapanos I, Aivalakis G. Gene transcript accumulation and enzyme activity of β-amylases suggest involvement in the starch depletion during the ripening of cherry tomatoes. Plant Gene, 2016, 5: 8–12
CrossRef Google scholar
[44]
Peroni F H, Koike C, Louro R P, Purgatto E, do Nascimento J R, Lajolo F M, Cordenunsi B R. Mango starch degradation. II. The binding of α-amylase and β-amylase to the starch granule. Journal of Agricultural and Food Chemistry, 2008, 56(16): 7416–7421
CrossRef Google scholar
[45]
Lao N T, Schoneveld O, Mould R M, Hibberd J M, Gray J C, Kavanagh T A. An Arabidopsis gene encoding a chloroplast-targeted β-amylase. Plant Journal, 1999, 20(5): 519–527
CrossRef Google scholar
[46]
Maeo K, Tomiya T, Hayashi K, Akaike M, Morikami A, Ishiguro S, Nakamura K. Sugar-responsible elements in the promoter of a gene for β-amylase of sweet potato. Plant Molecular Biology, 2001, 46(5): 627–637
CrossRef Google scholar
[47]
Gubler F, Jacobsen J V. Gibberellin-responsive elements in the promoter of a barley high-pI α-amylase gene. Plant Cell, 1992, 4(11): 1435–1441
[48]
Huttly A K, Phillips A L, Tregear J W. Localisation of cis elements in the promoter of a wheat α-Amy2 gene. Plant Molecular Biology, 1992, 19(6): 903–911
CrossRef Google scholar
[49]
Chan M T, Chang H H, Ho S L, Tong W F, Yu S M. Agrobacterium-mediated production of transgenic rice plants expressing a chimeric α-amylasepromoter/β-glucuronidase gene. Plant Molecular Biology, 1993, 22(3): 491–506
CrossRef Google scholar

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31401843), the Modern Agro-industry Technology Research System (CARS-32), the National Nonprofit Institute Research Grant of CATAS-ITBB (1630052016006), the National Program on Key Basic Research Project of China (2014CB160314), and the Natural Science Foundation of Hainan Province (314100).

Supplementary materials

The online version of this article at http://dx.doi.org/10.15302/J-FASE-2016127 contains supplementary materials (Appendix A).

Compliance with ethics guidelines

Hongxia Miao, Peiguang Sun, Yulu Miao, Juhua Liu, Jianbin Zhang, Caihong Jia, Jingyi Wang, Zhuo Wang, Zhiqiang Jin, and Biyu Xu declare that they have no conflict of interest or financial conflicts to disclose.
This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2016. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)
AI Summary AI Mindmap
PDF(1111 KB)

Accesses

Citations

Detail

Sections
Recommended

/