Comparative transcriptomics revealed enhanced light responses, energy transport and storage in domestication of cassava (Manihot esculenta)
Zhiqiang XIA, Xin CHEN, Cheng LU, Meiling ZOU, Shujuan WANG, Yang ZHANG, Kun PAN, Xincheng ZHOU, Haiyan WANG, Wenquan WANG
Comparative transcriptomics revealed enhanced light responses, energy transport and storage in domestication of cassava (Manihot esculenta)
Cassava is a staple food, feed and bioenergy crop important to the world especially in the tropics. Domesticated cassava is characterized by powerful carbohydrate accumulation but its wild progenitor is not. Here, we investigated the transcriptional differences of eight cDNA libraries derived from developing leaf, stem and storage root of cassava cv. Arg7 and an ancestor line, W14, using next generation sequencing system. A total of 41302 assembled transcripts were obtained and from these, 25961 transcripts with FPKM≥3 in at least one library were named the expressed genes. A total of 2117, 1963 and 3584 transcripts were found to be differentially expressed in leaf, stem and storage root (150 d after planting), respectively, between Arg7 and W14 and ascribed to 103, 93 and 119 important pathways in leaf, stem and storage root, respectively. The highlight of this work is that the genes involved in light response, such as those for photosystem I (PSA) and photosystem II (PSB), other genes involved in light harvesting, and some of the genes in the Calvin cycle of carbon fixation were specially upregulated in leaf. Genes for transport and also for key rate-limiting enzymes (PFK, PGK and PK, GAPDH) coupling ATP consumption in glycolysis pathway were predominantly expressed in stem, and genes for sucrose degradation (INVs), amylose synthesis (GBSS) and hydrolysis (RCP1, AMYs), the three key steps of starch metabolism, and transport associated with energy translocation (ABC, AVPs and ATPase) and their upstream transcription factors had enhanced expression in storage root in domesticated cassava. Co-expression networks among the pathways in each organs revealed the relationship of the genes involved, and uncovered some of the important hub genes and transcription factors targeting genes for photosynthesis, transportation and starch biosynthesis.
cassava / comparative transcriptomics / energy transport / photosynthesis / starch synthesis
[1] |
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
|
[2] |
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
|
[3] |
Olsen K M, Schaal B A. Evidence on the origin of cassava: phylogeography of Manihot esculenta. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96(10): 5586–5591
CrossRef
Google scholar
|
[4] |
Olsen K M, Schaal B A. Microsatellite variation in cassava (Manihot esculenta, Euphorbiaceae) and its wild relatives: further evidence for a southern Amazonian origin of domestication. American Journal of Botany, 2001, 88(1): 131–142
CrossRef
Google scholar
|
[5] |
Colombo C, Second G, Charrier A. Genetic relatedness between cassava (Manihot esculenta Crantz) and M. flabellifolia and M. Peruviana based on both RAPD and AFLP markers. Genetics and Molecular Biology, 2000, 23(2): 417–423
CrossRef
Google scholar
|
[6] |
Olsen K M. SNPs, SSRs and inferences on cassava’s origin. Plant Molecular Biology, 2004, 56(4): 517–526
CrossRef
Google scholar
|
[7] |
Pujol B, Mühlen G, Garwood N, Horoszowski Y, Douzery E J, McKey D. Evolution under domestication: contrasting functional morphology of seedlings in domesticated cassava and its closest wild relatives. New Phytologist, 2005, 166(1): 305–318
CrossRef
Google scholar
|
[8] |
Prochnik S, Marri P R, Desany B, Rabinowicz P D, Kodira C, Mohiuddin M, Rodriguez F, Fauquet C, Tohme J, Harkins T, Rokhsar D S, Rounsley S. The cassava genome: current progress, future directions. Tropical Plant Biology, 2012, 5(1): 88–94
CrossRef
Google scholar
|
[9] |
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
|
[10] |
Verdier V, Restrepo S, Mosquera G, Jorge V, Lopez C. Recent progress in the characterization of molecular determinants in the Xanthomonas axonopodis pv. manihotis-cassava interaction. Plant Molecular Biology, 2004, 56(4): 573–584
CrossRef
Google scholar
|
[11] |
Kemp B P, Beeching J R, Cooper R M. cDNA-AFLP reveals genes differentially expressed during the hypersensitive response of cassava. Molecular Plant Pathology, 2005, 6(2): 113–123
CrossRef
Google scholar
|
[12] |
Sojikul P, Kongsawadworakul P, Viboonjun U, Thaiprasit J, Intawong B, Narangajavana J, Svasti J. AFLP-based transcript profiling for cassava genome-wide expression analysis in the onset of storage root formation. Physiologia Plantarum, 2010, 140(2): 189–298
CrossRef
Google scholar
|
[13] |
Lopez C, Soto M, Restrepo S, Piégu B, Cooke R, Delseny M, Tohme J, Verdier V. Gene expression profile in response to Xanthomonas axonopodis pv. manihotis infection in cassava using a cDNA microarray. Plant Molecular Biology, 2005, 57(3): 393–410
CrossRef
Google scholar
|
[14] |
Utsumi Y, Tanaka M, Morosawa T, Kurotani A, Yoshida T, Mochida K, Matsui A, Umemura Y, Ishitani M, Shinozaki K, Sakurai T, Seki M. Transcriptome analysis using a high-density oligomicroarray under drought stress in various genotypes of cassava: an important tropical crop. DNA Research, 2012, 19(4): 335–345
CrossRef
Google scholar
|
[15] |
An D, Yang J, Zhang P. Transcriptome profiling of low temperature-treated cassava apical shoots showed dynamic responses of tropical plant to cold stress. BMC Genomics, 2012, 13(1): 64
CrossRef
Google scholar
|
[16] |
Reilly K, Bernal D, Cortes D F, Gomez-Vasquez R, Tohme J, Beeching J R. Towards identifying the full set of genes expressed during cassava post-harvest physiological deterioration. Plant Molecular Biology, 2007, 64(1–2): 187–203
CrossRef
Google scholar
|
[17] |
Gao Y, Xu H, Shen Y, Wang J. Transcriptomic analysis of rice (Oryza sativa) endosperm using the RNA-Seq technique. Plant Molecular Biology, 2013, 81(4–5): 363–378
CrossRef
Google scholar
|
[18] |
Oono Y, Kobayashi F, Kawahara Y, Yazawa T, Handa H, Itoh T, Matsumoto T. Characterization of the wheat (Triticum aestivum L.) transcriptome by de novo assembly for the discovery of phosphate starvation-responsive genes: gene expression in Pi-stressed wheat. BMC Genomics, 2013, 14(1): 77
CrossRef
Google scholar
|
[19] |
O’Rourke J A, Yang S S, Miller S S, Bucciarelli B, Liu J, Rydeen A, Bozsoki Z, Uhde-Stone C, Tu Z J, Allan D, Gronwald J W, Vance C P. An RNA-Seq transcriptome analysis of orthophosphate-deficient white lupin reveals novel insights into phosphorus acclimation in plants. Plant Physiology, 2013, 161(2): 705–724
CrossRef
Google scholar
|
[20] |
Allie F, Pierce E J, Okoniewski M J, Rey C. Transcriptional analysis of South African cassava mosaic virus-infected susceptible and tolerant landraces of cassava highlights differences in resistance, basal defense and cell wall associated genes during infection. BMC Genomics, 2014, 15(1): 1006
CrossRef
Google scholar
|
[21] |
El-Sharkawy M A. Cassava biology and physiology. Plant Molecular Biology, 2004, 56(4): 481–501
CrossRef
Google scholar
|
[22] |
McMaugh S J, Thistleton J L, Anschaw E, Luo J, Konik-Rose C, Wang H, Huang M, Larroque O, Regina A, Jobling S A, Morell M K, Li Z. Suppression of starch synthase I expression affects the granule morphology and granule size and fine structure of starch in wheat endosperm. Journal of Experimental Botany, 2014, 65(8): 2189–2201
CrossRef
Google scholar
|
[23] |
Tetlow I J, Morell M K, Emes M J. Recent developments in understanding the regulation of starch metabolism in higher plants. Journal of Experimental Botany, 2004, 55(406): 2131–2145
CrossRef
Google scholar
|
[24] |
Wang W, Feng B, Xiao J, Xia Z, Zhou X, Li P, Zhang W, Wang Y, Meller B L, Zhang P, Luo M C, Xiao G, Liu J, Yang J, Chen S, Rabinowicz P D, Chen X, Zhang H B, Ceballos H, Lou Q, Zou M, Carvalho L J, Zeng C, Xia J, Sun S, Fu Y, Wang H, Lu C, Ruan M, Zhou S, Wu Z, Liu H, Kannangara R M, Jorgensen K, Neale R L, Bonde M, Heinz N, Zhu W, Wang S, Zhang Y, Pan K, Wen M, Ma P A, Li Z, Hu M, Liao W, Hu W, Zhang S, Pei J, Guo A, Guo J, Zhang J, Zhang Z, Ye J, Ou W, Ma Y, Liu X, Tallon L J, Galens K, Ott S, Huang J, Xue J, An F, Yao Q, Lu X, Fregene M, Lopez-Lavalle L A, Wu J, You F M, Chen M, Hu S, Wu G, Zhong S, Ling P, Chen Y, Wang Q, Liu G, Liu B, Li K, Peng M. Cassava genome from a wild ancestor to cultivated varieties. Nature Communications, 2014, 10(5): 5110
CrossRef
Google scholar
|
[25] |
Zhong S L, Joung J G, Zheng Y, Chen Y R, Liu B, Shao Y, Xiang J Z, Fei Z J, Giovannoni J J. High-throughput Illumina strand-specific RNA sequencing library preparation. Cold Spring Harbor Protocols, 2011, 2011(8): 940–949
CrossRef
Google scholar
|
[26] |
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
|
[27] |
Quevillon, E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R.InterProScan: protein domains identifier. Nucleic Acids Research, 2005, 33(Suppl. 2): W116–W120
|
[28] |
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J.WEGO: a web tool for plotting GO annotations. Nucleic Acids Research, 2006, 34(Suppl. 2): W293–W297
|
[29] |
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y. KEGG for linking genomes to life and the environment. Nucleic Acids Research, 2008, 36(Suppl. 1): D480–D484
|
[30] |
Patrick E, Meyer, Frederic L, Gianluca B. minet: A R/Bioconductor package for inferring large transcriptional networks using mutual information. BMC Bioinformatics, 2008, 9(1): 461
|
[31] |
Engelmann S, Bläsing O E, Gowik U, Svensson P, Westhoff P. Molecular evolution of C4 phosphoenol-pyruvate carboxylase in the genus Flaveria–a gradual increase from C3 to C4 characteristics. Planta, 2003, 217(5): 717–725
CrossRef
Google scholar
|
[32] |
Gowik U, Bräutigam A, Weber K L, Weber A P, Westhoff P. Evolution of C4 photosynthesis in the genus Flaveria: how many and which genes does it take to make C4? Plant Cell, 2011, 23(6): 2087–2105
CrossRef
Google scholar
|
[33] |
Sakurai T, Plata G, Rodriguez-Zapata F, Seki M, Salcedo A, Toyoda A, Ishiwata A, Tohme J, Sakaki Y, Shinozaki K, Ishitani M, eIshiwata A, Tohme J, Sakaki Y, Shinozaki K, Ishitani M. Sequencing analysis of 20000 full-length cDNA clones from cassava reveals lineage specific expansions in gene families related to stress response. BMC Plant Biology, 2007, 7(1): 66
CrossRef
Google scholar
|
[34] |
Ding Z H, Zhang Y, Xiao Y, Liu F F, Wang M H, Zhu X G, Liu P, Sun Q, Wang W Q, Peng M, Tom Brutnell & Li P H. Transcriptome response of cassava leaves under natural shade. Scientific Reports, 2016, 6: 31673
CrossRef
Google scholar
|
[35] |
Li Y Z, Zhao J Y, Wu S M, Fan X W, Luo X L, Chen B S. Characters related to higher starch accumulation in cassava storage roots. Scientific Reports, 2016, 6: 19823
CrossRef
Google scholar
|
[36] |
Wang X C, Chang L L, Tong Z, Wang D Y, Yin Q, Wang D, Jin X, Yang Q, Wang L M, Sun Y, Huang Q X, Guo A P, Peng M. Proteomics profling reveals carbohydrate metabolic enzymes and 14–3–3 proteins play important roles for starch accumulation during cassava root tuberization. Scientific Reports, 2016, 6: 19643
CrossRef
Google scholar
|
[37] |
Kang G, Liu G, Peng X, Wei L, Wang C, Zhu Y, Ma Y, Jiang Y, Guo T. Increasing the starch content and grain weight of common wheat by over-expression of the cytosolic AGPase large subunit gene. Plant Physiology & Biochemistry Ppb, 2013, 73(6): 93–98
CrossRef
Google scholar
|
[38] |
Asare E K, Båga M, Rossnagel B G, Chibbar R N. Polymorphism in the barley granule-bound starch synthase 1 (gbss1) gene associated with grain starch variant amylose concentration. Journal of Agricultural and Food Chemistry, 2012, 60(40): 10082–10092
CrossRef
Google scholar
|
/
〈 | 〉 |