Abstract
Traits related to grain and reproductive organs in grass crops have been under continuous directional selection during domestication. Barley is one of the oldest domesticated crops in human history. Thus genes associated with the grain and reproductive organs in barley may show evidence of dramatic evolutionary change. To understand how artificial selection contributes to protein evolution of biased genes in different barley organs, we used Digital Gene Expression analysis of six barley organs (grain, pistil, anther, leaf, stem and root) to identify genes with biased expression in specific organs. Pairwise comparisons of orthologs between barley and Brachypodium distachyon, as well as between highland and lowland barley cultivars mutually indicated that grain and pistil biased genes show relatively higher protein evolutionary rates compared with the median of all orthologs and other organ biased genes. Lineage-specific protein evolutionary rates estimation showed similar patterns with elevated protein evolution in barley grain and pistil biased genes, yet protein sequences generally evolve much faster in the lowland barley cultivar. Further functional annotations revealed that some of these grain and pistil biased genes with rapid protein evolution are related to nutrient biosynthesis and cell cycle/division. Our analyses provide insights into how domestication differentially shaped the evolution of genes specific to different organs of a crop species, and implications for future functional studies of domestication genes.
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References
Abascal F, Zardoya R, Telford MJ (2010) TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 38:W7–W13
Abbo S, Pinhasi VR, Gopher A, Saranga Y, Ofner I, Peleg Z (2014) Plant domestication versus crop evolution: a conceptual framework for cereals and grain legumes. Trends Plant Sci 19:351–360
Akhunov ED, Sehgal S, Liang H, Wang S, Akhunova AR, Kaur G, Li W, Forrest KL, See D, Simkova H, Ma Y, Hayden MJ, Luo M, Faris JD, Dolezel J, Gill BS (2013) Comparative analysis of syntenic genes in grass genomes reveals accelerated rates of gene structure and coding sequence evolution in polyploid wheat. Plant Physiol 161:252–265
Arunkumar R, Josephs EB, Williamson RJ, Wright SI (2013) Pollen-specific, but not sperm-specific, genes show stronger purifying selection and higher rates of positive selection than sporophytic genes in Capsella grandiflora. Mol Biol Evol 30:2475–2486
Azhaguvel P, Komatsuda T (2007) A phylogenetic analysis based on nucleotide sequence of a marker linked to the brittle rachis locus indicates a diphyletic origin of barley. Ann Bot 100:1009–1015
Baud S, Dichow NR, Kelemen Z, D’Andrea S, To A, Berger N, Canonge M, Kronenberger J, Viterbo D, Dubreucq B, Lepiniec L, Chardot T, Miquel M (2009) Regulation of HSD1 in seeds of Arabidopsis thaliana. Plant Cell Physiol 50:1463–1478
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Cruz F, Vila C, Webster MT (2008) The legacy of domestication: accumulation of deleterious mutations in the dog genome. Mol Biol Evol 25:2331–2336
Dai F, Nevo E, Wu D, Comadran J, Zhou M, Qiu L, Chen Z, Beiles A, Chen G, Zhang G (2012) Tibet is one of the centers of domestication of cultivated barley. Proc Natl Acad Sci USA 109:16969–16973
Dai F, Chen ZH, Wang X, Li Z, Jin G, Wu D, Cai S, Wang N, Wu F, Nevo E, Zhang G (2014) Transcriptome profiling reveals mosaic genomic origins of modern cultivated barley. Proc Natl Acad Sci USA 111:13403–13408
Du Z, Hou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70
Finseth FR, Bondra E, Harrison RG (2014) Selective constraint dominates the evolution of genes expressed in a novel reproductive gland. Mol Biol Evol 31:3266–3281
Glemin S, Bataillon T (2009) A comparative view of the evolution of grasses under domestication. New Phytol 183:273–290
Gossmann TI, Schmid MW, Grossniklaus U, Schmid KJ (2014) Selection-driven evolution of sex-biased genes is consistent with sexual selection in Arabidopsis thaliana. Mol Biol Evol 31:574–583
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652
Gruis DF, Selinger DA, Curran JM, Jung R (2002) Redundant proteolytic mechanisms process seed storage proteins in the absence of seed-type members of the vacuolar processing enzyme family of cysteine proteases. Plant Cell 14:2863–2882
Harlan JR, Zohary D (1966) Distribution of wild wheats and barley. Science 153:1074–1080
Helback H (1959) Domestication of food plants in the old world: joint efforts by botanists and archeologists illuminate the obscure history of plant domestication. Science 130:365–372
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664
Knüpffer H, Terentyeva I, Hammer K, Kovaleva O, Sato K (2003) Chapter 4 Ecogeographical diversity—a Vavilovian appraoch. In: RolandVon Bothmer TVHH (ed) Developments in plant genetics and breeding. Elsevier, Amsterdam, pp 53–76
Koenig D, Jimenez-Gomez JM, Kimura S, Fulop D, Chitwood DH, Headland LR, Kumar R, Covington MF, Devisetty UK, Tat AV, Tohge T, Bolger A, Schneeberger K, Ossowski S, Lanz C, Xiong G, Taylor-Teeples M, Brady SM, Pauly M, Weigel D, Usadel B, Fernie AR, Peng J, Sinha NR, Maloof JN (2013) Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proc Natl Acad Sci USA 110:E2655–E2662
Komatsuda T, Pourkheirandish M, He C, Azhaguvel P, Kanamori H, Perovic D, Stein N, Graner A, Wicker T, Tagiri A, Lundqvist U, Fujimura T, Matsuoka M, Matsumoto T, Yano M (2007) Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc Natl Acad Sci USA 104:1424–1429
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25
Liu T, Tang S, Zhu S, Tang Q, Zheng X (2014) Transcriptome comparison reveals the patterns of selection in domesticated and wild ramie (Boehmeria nivea L. Gaud). Plant Mol Biol 86:85–92
Lu J, Tang T, Tang H, Huang J, Shi S, Wu CI (2006) The accumulation of deleterious mutations in rice genomes: a hypothesis on the cost of domestication. Trends Genet 22:126–131
Mayer KF, Waugh R, Brown JW, Schulman A, Langridge P, Platzer M, Fincher GB, Muehlbauer GJ, Sato K, Close TJ, Wise RP, Stein N (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716
Meyer RS, Purugganan MD (2013) Evolution of crop species: genetics of domestication and diversification. Nat Rev Genet 14:840–852
Min XJ, Butler G, Storms R, Tsang A (2005) OrfPredictor: predicting protein-coding regions in EST-derived sequences. Nucleic Acids Res 33:W677–W680
Morrell PL, Clegg MT (2007) Genetic evidence for a second domestication of barley (Hordeum vulgare) east of the Fertile Crescent. Proc Natl Acad Sci USA 104:3289–3294
Oliver TA, Garfield DA, Manier MK, Haygood R, Wray GA, Palumbi SR (2010) Whole-genome positive selection and habitat-driven evolution in a shallow and a deep-sea urchin. Genome Biol Evol 2:800–814
Pietra S, Gustavsson A, Kiefer C, Kalmbach L, Horstedt P, Ikeda Y, Stepanova AN, Alonso JM, Grebe M (2013) Arabidopsis SABRE and CLASP interact to stabilize cell division plane orientation and planar polarity. Nat Commun 4:2779
Proost S, Van Bel M, Vaneechoutte D, Van de Peer Y, Inze D, Mueller-Roeber B, Vandepoele K (2015) PLAZA 3.0: an access point for plant comparative genomics. Nucleic Acids Res 43:D974–D981
Purugganan MD, Fuller DQ (2009) The nature of selection during plant domestication. Nature 457:843–848
Ragel P, Streb S, Feil R, Sahrawy M, Annunziata MG, Lunn JE, Zeeman S, Merida A (2013) Loss of starch granule initiation has a deleterious effect on the growth of arabidopsis plants due to an accumulation of ADP-glucose. Plant Physiol 163:75–85
Ramsay L, Comadran J, Druka A, Marshall DF, Thomas WT, Macaulay M, MacKenzie K, Simpson C, Fuller J, Bonar N, Hayes PM, Lundqvist U, Franckowiak JD, Close TJ, Muehlbauer GJ, Waugh R (2011) INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1. Nat Genet 43:169–172
Rasmusson DC, Wilcoxson RW (1979) Registration of Morex Barley1 (Reg. No. 158). Crop Sci 19:293
Shamir R, Maron-Katz A, Tanay A, Linhart C, Steinfeld I, Sharan R, Shiloh Y, Elkon R (2005) EXPANDER—an integrative program suite for microarray data analysis. BMC Bioinform 6:232
Taketa S, Amano S, Tsujino Y, Sato T, Saisho D, Kakeda K, Nomura M, Suzuki T, Matsumoto T, Sato K, Kanamori H, Kawasaki S, Takeda K (2008) Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway. Proc Natl Acad Sci USA 105:4062–4067
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
Tzafrir I, McElver JA, Liu CC, Yang LJ, Wu JQ, Martinez A, Patton DA, Meinke DW (2002) Diversity of TITAN functions in Arabidopsis seed development. Plant Physiol 128:38–51
Ulitsky I, Maron-Katz A, Shavit S, Sagir D, Linhart C, Elkon R, Tanay A, Sharan R, Shiloh Y, Shamir R (2010) Expander: from expression microarrays to networks and functions. Nat Protoc 5:303–322
Vogel JPGDMT (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768
Wang Z, Yonezawa T, Liu B, Ma T, Shen X, Su J, Guo S, Hasegawa M, Liu J (2011) Domestication relaxed selective constraints on the yak mitochondrial genome. Mol Biol Evol 28:1553–1556
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591
Yang L, Gaut BS (2011) Factors that contribute to variation in evolutionary rate among Arabidopsis genes. Mol Biol Evol 28:2359–2369
Yang P, Liu X, Liu X, Yang W, Feng Z (2010) Diversity analysis of the developed qingke (hulless barley) cultivars representing different growing regions of the Qinghai-Tibet Plateau in China using sequence-related amplified polymorphism (SRAP) markers. Afr J Biotechnol 9:8530–8538
Zeng X, Long H, Wang Z, Zhao S, Tang Y, Huang Z, Wang Y, Xu Q, Mao L, Deng G, Yao X, Li X, Bai L, Yuan H, Pan Z, Liu R, Chen X, WangMu Q, Chen M, Yu L, Liang J, DunZhu D, Zheng Y, Yu S, LuoBu Z, Guang X, Li J, Deng C, Hu W, Chen C, TaBa X, Gao L, Lv X, Abu YB, Fang X, Nevo E, Yu M, Wang J, Tashi N (2015) The draft genome of Tibetan hulless barley reveals adaptive patterns to the high stressful Tibetan Plateau. Proc Natl Acad Sci USA 112:1095–1100
Acknowledgments
We thank Dr. Jianquan Liu (Lanzhou University) for providing server on computational analyses and Kun Wang (Lanzhou University) for managing technical issues related to computational analyses on the server. We thank Wendy Chen (Lanzhou University) for reading and giving comments on the paper. This work was supported by the National Basic Research Program of China [Grant 2011CB915401 to Jia Li], the National Natural Science Foundation of China [Grant 91317311 to Jia Li], and China Postdoctoral Science Foundation [Grant 132867 to Tao Shi].
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Shi, T., Dimitrov, I., Zhang, Y. et al. Accelerated rates of protein evolution in barley grain and pistil biased genes might be legacy of domestication. Plant Mol Biol 89, 253–261 (2015). https://doi.org/10.1007/s11103-015-0366-2
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DOI: https://doi.org/10.1007/s11103-015-0366-2