Annotation and validation of genes involved in photosynthesis and starch synthesis from a Manihot full-length cDNA library

Yang ZHANG, Xin CHEN, Haiyan WANG, Zhiqiang XIA, Peng LING, Wenquan WANG

PDF(1205 KB)
PDF(1205 KB)
Front. Agr. Sci. Eng. ›› 2016, Vol. 3 ›› Issue (4) : 308-320. DOI: 10.15302/J-FASE-2016113
RESEARCH ARTICLE
RESEARCH ARTICLE

Annotation and validation of genes involved in photosynthesis and starch synthesis from a Manihot full-length cDNA library

Author information +
History +

Abstract

A full-length cDNA library from leaf and root tissues of cassava (Manihot esculenta) Arg7 and one accession of its wild ancestor W14 (M. esculenta ssp. flabellifolia) has been constructed. The library is comprised of four sub-libraries, containing 32640 recombinant clones, 6028 cDNA clones from their 5′ ends, and 128 clones from the 3′ ends were sequenced. In total, 5013 high-quality expressed sequence tags (ESTs) and 1259 unigenes were obtained. Of these, 746 unigenes were identified by their sequence homologies to ESTs from model plants, and 323 unigenes were mapped onto 114 different KEGG pathways. From these, 24 differentially expressed genes involved in starch metabolism and photosynthesis were identified and five of them were selected to compare their expression level between Arg7 and W14. Notably, Arg7 has a higher net photosynthesis rate in leaves, higher ribulose-1,5-bisphosphate carboxy-lase oxygenase activities in leaves, and higher AGPase activity in roots. This resource is the first EST collection from wild cassava and should be of value for gene discovery, genome annotation and studies of Manihot evolution.

Keywords

Manihot esculenta / expressed sequence tag / unigene / pathway / expression pattern

Cite this article

Download citation ▾
Yang ZHANG, Xin CHEN, Haiyan WANG, Zhiqiang XIA, Peng LING, Wenquan WANG. Annotation and validation of genes involved in photosynthesis and starch synthesis from a Manihot full-length cDNA library. Front. Agr. Sci. Eng., 2016, 3(4): 308‒320 https://doi.org/10.15302/J-FASE-2016113

References

[1]
Taylor N, Chavarriaga P, Raemakers K, Siritunga D, Zhang P. Development and application of transgenic technologies in cassava. Plant Molecular Biology, 2004, 56(4): 671–688
CrossRef Google scholar
[2]
de Souza C R B, Carvalho L J C B, de Mattos Cascardo J C. Comparative gene expression study to identify genes possibly related to storage root formation in cassava. Protein and Peptide Letters, 2004, 11(6): 577–582
CrossRef Google scholar
[3]
Koch B, Sibbesen O, Swain E, Kahn R, Liangcheng D, Bak S, Halkier B, Møller B. Possible use of a biotechnological approach to optimize and regulate the content and distribution of cyanogenic glycosides in cassava to increase food safety. Acta Horticulturae, 1994, (375): 45–60
CrossRef Google scholar
[4]
Siritunga D, Sayre R T. Domestication of cassava: generation of cyanogen-free cassava. Planta, 2003, 217(3): 367–373
CrossRef Google scholar
[5]
Jansson C, Westerbergh A, Zhang J, Hu X W, Sun C. Cassava, a potential biofuel crop in the People’s Republic of China. Applied Energy, 2009, 86(S1): S95–S99
CrossRef Google scholar
[6]
Ziska L H, Runion G B, Tomecek M, Prior S A, Torbet H A, Sicher R. An evaluation of cassava, sweet potato and field corn as potential carbohydrate sources for bio-ethanol production in Alabama and Maryland. Biomass and Bioenergy, 2009, 33(11): 1503–1508
CrossRef Google scholar
[7]
Hunt C A, Wholey D M, Cock J H. Growth physiology of cassava (Manihot esculenta Crantz). Field Crop Abstracts, 1977, 30: 77–89
[8]
Edwards G E, Sheta E, Moore B D, Dai Z, Fransceschi V R, Cheng S H, Lin C H, Ku M S B. Photosynthetic characteristics of cassava (Manihot esculenta), a C3 species with chlorenchymatous bundle sheath cells. Plant & Cell Physiology, 1990, 31(8): 1199–1206
[9]
Angelov M N, Sun J, Byrd G T, Brown R H, Black C C. Novel characteristics of cassava, Manihot esculenta Crantz, a reputed C3–C4 intermediate photosynthesis species. Photosynthesis Research, 1993, 38(1): 61–72
CrossRef Google scholar
[10]
EI-Sharkawy M A. International research on cassava photosynthesis, productivity, eco-physiology, and responses to environmental stresses in the tropics. Photosynthetica, 2006, 44(4): 481–512
[11]
Osunsami A T, Akingbala J O, Oguntimein G B. Effect of storage on starch content and modification of cassava starch. Starch, 1989, 41(2): 54–57
CrossRef Google scholar
[12]
Lopez C, Jorge V, Piegu B, Mba C, Cortes D, Restrepo S, Soto M, Laudie M, Berger C, Cooke R, Delseny M, Tohme J, Verdier V. An unigene catalogue of 5700 expressed genes in cassava. Plant Molecular Biology, 2004, 56(4): 541–554
CrossRef Google scholar
[13]
Lokko Y, Anderson J V, Rudd S, Raji A, Horvath D, Mikel M A, Kim R, Liu L, Hernandez A, Dixon A G, Ingelbrecht I L. Characterization of an 18166 EST dataset for cassava (Manihot esculenta Crantz) enriched for drought-responsive genes. Plant Cell Reports, 2007, 26(9): 1605–1618
CrossRef Google scholar
[14]
Sakurai T, Plata G, Rodriguez-Zapata F, Seki M, Salcedo A, Toyoda A, Ishiwata A, Tohme J, Sakaki Y, Shinozaki K, Ishitani M. Sequencing analysis of 20,000 full-length cDNA clones from cassava reveals lineage specific expansions in gene families related to stress response. BMC Plant Biology, 2007, 7: 66
CrossRef Google scholar
[15]
Li Y Z, Pan Y H, Sun C B, Dong H T, Luo X L, Wang Z Q, Tang J L, Chen B. An ordered EST catalogue and gene expression profiles of cassava (Manihot esculenta) at key growth stages. Plant Molecular Biology, 2010, 74(6): 573–590
CrossRef Google scholar
[16]
Robert J S, Michael E S. RUBISCO: structure, regulatory interactions, and possibilities for a better enzyme. Annual Review of Plant Biology, 2002, 53(4): 449–475
[17]
Allen J F. Oxygen reduction and optimum production of ATP in photosynthesis. Nature, 1975, 256(5518): 599–600
CrossRef Google scholar
[18]
Bandyopadhyay A, Datta K, Zhang J, Yang W, Raychaudhuri S, Miyao M, Datta S K. Enhanced photosynthesis rate in genetically engineered indica rice expressing pepc gene cloned from maize. Plant Science, 2007, 172(6): 1204–1209
CrossRef Google scholar
[19]
Chollet R, Vidal J, O’Leary M H. Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 1996, 47(1): 273–298
CrossRef Google scholar
[20]
Yoshihara N, Imayama T, Fukuchi-Mizutani M, Okuhara H, Tanaka Y, Ino I, Yabuya T. cDNA cloning and characterization of UDP-glucose: anthocyanidin 3-O-glucosyltransferase in Iris hollandica. Plant Science, 2005, 169(3): 496–501
CrossRef Google scholar
[21]
Tomlinson P T, Duke E R, Nolte K D, Koch K E. Sucrose synthase and invertase in isolated vascular bundles. Plant Physiology, 1991, 97(3): 1249–1252
CrossRef Google scholar
[22]
Fernie A R, Willmitzer L, Trethewey R N. Sucrose to starch: a transition in molecular plant physiology. Trends in Plant Science, 2002, 7(1): 35–41
CrossRef Google scholar
[23]
Kleczkowski L A. Is leaf ADP-glucose pyrophosphorylase an allosteric enzyme? Biochimica et Biophysica Acta (BBA)-Protein Structure and Molecular Enzymology, 2000, 1476(1): 103–108
CrossRef Google scholar
[24]
Kleczkowski L A. A new player in the starch field. Plant Physiology and Biochemistry, 2001, 39(9): 759–761
CrossRef Google scholar
[25]
Stam M, Mol J N M, Kooter J M. The silence of genes in transgenic plants. Annals of Botany, 1997, 79(1): 3–12
CrossRef Google scholar
[26]
Zhu Y Y, Machleder E M, Chenchik A, Li R, Siebert P D. Reverse transcriptase template switching: a SMARTTM approach for full-length cDNA library construction. BioTechniques, 2001, 30(4): 892–897
[27]
Ewing B, Green P. Base-calling of automated sequencer traces using Phred. II. Error probabilities. Genome Research, 1998, 8(3): 186–194
CrossRef Google scholar
[28]
Ewing B, Hillier L D, Wendl M C, Green P. Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Research, 1998, 8(3): 175–185
CrossRef Google scholar
[29]
Zhang Z, Schwartz S, Wagner L, Miller W.A greedy algorithm for aligning DNA sequences. Journal of Computational Biology, 2000, 7(1–2): 203–214
[30]
Huang X, Madan A. CAP3: a DNA sequence assembly program. Genome Research, 1999, 9(9): 868–877
CrossRef Google scholar
[31]
Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J. TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics, 2003, 19(5): 651–652
CrossRef Google scholar
[32]
Camon E, Barrell D, Lee V, Dimmer E, Apweiler R. The gene ontology annotation (GOA) database-an integrated resource of GO annotations to the UniProt knowledgebase. In Silico Biology, 2004, 4(4): 5–6
[33]
El-Sharkawy M A, Cock J H, de Cadena G. Influence of differences in leaf anatomy on net photosynthetic rates of some cultivars of cassava. Photosynthesis Research, 1984, 5(3): 235–242
CrossRef Google scholar
[34]
Mullikin J C, McMurray A A. Sequencing the genome, fast. Science, 1999, 283(5409): 1867–1868
CrossRef Google scholar
[35]
Angelov M N, Sun J, Byrd G T, Brown R H, Black C C. Novel characteristics of cassava, Manihot esculenta Crantz, a reputed C3–C4 intermediate photosynthesis species. Photosynthesis Research, 1993, 38(1): 61–72
CrossRef Google scholar
[36]
Zeeman S C, Smith S M, Smith A M. The diurnal metabolism of leaf starch. Biochemical Journal, 2007, 401(1): 13–28
CrossRef Google scholar
[37]
Zeeman S C, Kossmann J, Smith A M. Starch: its metabolism, evolution, and biotechnological modification in plants. Annual Review of Plant Biology, 2010, 61(1): 209–234
CrossRef Google scholar
[38]
Estruch J J, Beltrán J P. Change in invertase activities precede ovary growth induced by gibberellic acid in Pisum sativum. Physiologia Plantarum, 1991, 81(3): 319–326
CrossRef Google scholar
[39]
Geigenberger P, Stitt M. Diurnal changes in sucrose, nucleotides, starch synthesis and AGPs transcript in growing potato tubers that are suppressed by decreased expression of sucrose phosphate synthase. Plant Journal, 2000, 23(6): 795–806
CrossRef Google scholar
[40]
Gerhardt R, Stitt M, Heldt H W. Subcellular metabolite levels in spinach leaves. Plant Physiology, 1987, 83(2): 399–407
CrossRef Google scholar
[41]
Ying W H. NAD+/NADH and NADP+/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxidants & Redox Signalling, 2008, 10(2): 179–206
CrossRef Google scholar
[42]
Schulze J, Shi L F, Blumenthal J, Samac D A, Gantt J S, Vance C P. Inhibition of alfalfa root nodule phosphoenolpyruvate carboxylase through an antisense strategy impacts nitrogen fixation and plant growth. Phytochemistry, 1998, 49(2): 341–346
CrossRef Google scholar
[43]
Begum H H, Osaki M, Shinano T, Miyatake H, Wasaki J, Yamamura T, Watanabe T. The function of a maize-derived phosphoenol pyruvate carboxylase (PEPC) in phosphorus-deficient transgenic rice. Soil Science and Plant Nutrition, 2005, 51(4): 497–506
CrossRef Google scholar
[44]
Munyikwa T, Kreuze J, Fregene M, Suurs L, Jacobsen E, Visser R. Isolation and characterisation of cDNAs encoding the large and small subunits of ADP-glucose pyrophosphorylase from cassava (Manihot esculenta Crantz). Euphytica, 2001, 120(1): 71–83
CrossRef Google scholar
[45]
Ihemere U, Arias-Garzon D, Lawrence S, Sayre R. Genetic modification of cassava for enhanced starch production. Plant Biotechnology, 2006, 4(4): 453–465
CrossRef Google scholar
[46]
Ausubel F M. Are innate immune signaling pathways in plants and animals conserved? Nature Immunology, 2005, 6(10): 973–979
CrossRef Google scholar
[47]
Oh C S, Pedley K F, Martin G B. Tomato 14–3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK a. Plant Cell, 2010, 22(1): 260–272
CrossRef Google scholar
[48]
Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nature Reviews Genetics, 2009, 10(1): 57–63
CrossRef Google scholar
[49]
Azcón-Bieto J, Lambers H, Day D A. Effect of photosynthesis and carbohydrate status on respiratory rates and the involvement of the alternative pathway in leaf respiration. Plant Physiology, 1983, 72(3): 598–603
CrossRef Google scholar
[50]
El-Sharkawy M A, Cock J H, Held A A. Photosynthetic responses of cassava cultivars (Manihot esculenta Crantz) from different habitats to temperature. Photosynthesis Research, 1984, 5(3): 243–250
CrossRef Google scholar
[51]
Tiessen A, Hendriks J H M, Stitt M, Branscheid A, Gibon Y, Farré E M, Geigenberger P. Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP–Glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell, 2002, 14(9): 2191–2213
CrossRef Google scholar
[52]
Calatayud P A, Barón C H, Velásquez H, Arroyave J A, Lamaze T. Wild Manihot species do not possess C4 photosynthesis. Annals of Botany, 2002, 89(1): 125–127
CrossRef Google scholar
[53]
Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell, 2001, 13(1): 61–72
CrossRef Google scholar

Acknowledgements

This work was supported by a National Nonprofit Institute Research Grant of CATAS-ITBB, and the earmarked fund for China Agricultural Research System (CARS-12). We thank Prof. Peng Zhang of Chinese Academy of Sciences for his constructive suggestions on this research.

Supplementary materials

The online version of this article at http://dx.doi.org/10.15302/J-FASE-2016113 contains supplementary material (Appendix A).

Compliance with ethics guidelines

The authors Yang Zhang, Xin Chen, Haiyan Wang, Zhiqiang Xia, Peng Ling, and Wenquan Wang declare that they have no conflicts 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(1205 KB)

Accesses

Citations

Detail

Sections
Recommended

/