Please wait a minute...
Journal of Integrative Agriculture  2015, Vol. 14 Issue (1): 42-49    DOI: 10.1016/S2095-3119(14)60821-2
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
Identification of microRNAs in two species of tomato, Solanum lycopersicum and Solanum habrochaites, by deep sequencing
 FAN Shan-shan, LI Qian-nan, GUO Guang-jun, GAO Jian-chang, WANG Xiao-xuan, GUO Yanmei, John C. Snyder, DU Yong-chen
1、Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
2、Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100094, P.R.China
3、Graduate School of Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
4、Department of Agronomy, University of Kentucky, Lexington, Kentucky 40546-0091, USA
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  MicroRNAs (miRNAs) are ~21 nucleotide (nt), endogenous RNAs that regulate gene expression in plants. Increasing evidence suggests that miRNAs play an important role in species-specific development in plants. However, the detailed miRNA profile divergence has not been performed among tomato species. In this study, the small RNA (sRNA) profiles of Solanum lycopersicum cultivar 9706 and Solanum habrochaites species PI 134417 were obtained by deep sequencing. Sixty-three known miRNA families were identified from these two species, of which 39 were common. Further miRNA profile comparison showed that 24 known non-conserved miRNA families were species-specific between these two tomato species. In addition, six conserved miRNA families displayed an apparent divergent expression pattern between the two tomato species. Our results suggested that species-specific, non-conserved miRNAs and divergent expression of conserved miRNAs might contribute to developmental changes and phenotypic variation between the two tomato species. Twenty new miRNAs were also identified in S. lycopersicum. This research significantly increases the number of known miRNA families in tomato and provides the first set of small RNAs in S. habrochaites. It also suggests that miRNAs have an important role in species-specific plant developmental regulation.

Abstract  MicroRNAs (miRNAs) are ~21 nucleotide (nt), endogenous RNAs that regulate gene expression in plants. Increasing evidence suggests that miRNAs play an important role in species-specific development in plants. However, the detailed miRNA profile divergence has not been performed among tomato species. In this study, the small RNA (sRNA) profiles of Solanum lycopersicum cultivar 9706 and Solanum habrochaites species PI 134417 were obtained by deep sequencing. Sixty-three known miRNA families were identified from these two species, of which 39 were common. Further miRNA profile comparison showed that 24 known non-conserved miRNA families were species-specific between these two tomato species. In addition, six conserved miRNA families displayed an apparent divergent expression pattern between the two tomato species. Our results suggested that species-specific, non-conserved miRNAs and divergent expression of conserved miRNAs might contribute to developmental changes and phenotypic variation between the two tomato species. Twenty new miRNAs were also identified in S. lycopersicum. This research significantly increases the number of known miRNA families in tomato and provides the first set of small RNAs in S. habrochaites. It also suggests that miRNAs have an important role in species-specific plant developmental regulation.
Keywords:  microRNAs       Solanum lycopersicum       Solanum habrochaites       deep sequencing  
Received: 13 February 2014   Accepted:
Fund: 

This work was supported by the National Basic Research Program of China (2009CB11900) and the Special Fund for Agro-Scientific Research in the Public Interest, China (201003065).

Corresponding Authors:  DU Yongchen,Fax: +86-10-62174123, E-mail: duyongchen@caas.cn     E-mail:  duyongchen@caas.cn
About author:  FAN Shan-shan, E-mail: fanshanshan_nine@126.com;* These authors contributed equally to this study

Cite this article: 

FAN Shan-shan, LI Qian-nan, GUO Guang-jun, GAO Jian-chang, WANG Xiao-xuan, GUO Yanmei, John C. Snyder, DU Yong-chen. 2015. Identification of microRNAs in two species of tomato, Solanum lycopersicum and Solanum habrochaites, by deep sequencing. Journal of Integrative Agriculture, 14(1): 42-49.

Allen E, Xie Z X, Gustafson A M, Carrington J C. 2005.microRNA-directed phasing during trans-acting sirnabiogenesis in plants. Cell, 2, 207 -221.

Ambros V, Bartel B, Bartel D P, Burge C B, Carrington J C, ChenX M, Dreyfuss G, Eddy S R, Griffiths-Jones S, Marshall M,Matzke M, Ruvkun G, Tuschl T. 2003. A uniform systemfor microRNA annotation. RNA, 9, 277-279

Bartel D P. 2004. MicroRNAs: Genomics, biogenesis,mechanism, and function. Cell, 116, 281-297.

Borsani O, hu J H, Verslues P E, Sunkar R, Zhu J K. 2005.Endogenous siRNAs derived from a pair of natural cisantisensetranscripts regulate salt tolerance in arabidopsis.Cell, 123, 1279-1291

Burkhead J L, Kathryn A. Gogolin Reynolds K A G, SalahE. Abdel-Ghany, Cohu C M, Pilon M. 2009. Copperhomeostasis. New Phytologist, 182, 799-816.

Cagas C C, Nemoto K, Sugiyama N. 2008. Quantitativetrait loci controlling flowering time and related traits in aSolanum lycopersicum× S. pimpinellifolium cross. ScientiaHorticulturae, 116, 144-151

Cai X, Davis E J, Ballif J, Liang M, Bushman E, HaroldsenV, Torabinejad J, Wu Y. 2006. Mutant identification andcharacterization of the laccase gene family in Arabidopsis.Journal of Experimental Botany, 57, 2563-2569.

Chen X M. 2004. A microRNA as a translational repressor ofAPETALA2 in Arabidopsis flower development. Science,303, 2022-2025

Chisholm S T, Coaker G, Day B, Staskawicz B J. 2006. Hostmicrobeinteractions: Shaping the evolution of the plantimmune response. Cell, 124, 803-814.

Dalmay T. 2011. Short RNAs in tomato. Journal of IntegrativePlant Biology, 52, 388-392

Shivaprasad P V, Chen H M, Patel K, Bond D M, Santos B A,Baulcombe D C. 2012. A microRNA superfamily regulatesnucleotide binding site-leucine-rich repeats and othermRNAs. The Plant Cell, 24, 859-874.

Fahlgren N, Howell M D, Kasschau K D, Chapman E J, SullivanC M, Cumbie J S, Givan S A, Law T F, Grant S R, DanglJ L, Carrington J C. 2007. High-throughput sequencing ofArabidopsis microRNAs: Evidence for frequent birth anddeath of MIRNA genes. PLoS ONE, 2, e219.

Feng H, Zhang Q, Wang Q L, Wang X J, Liu J, Li M, Huang LL, Kang Z H. 2013. Target of tae-miR408, a chemocyaninlikeprotein gene (TaCLP1), plays positive roles in wheatresponse to high-salinity, heavy cupric stress and striperust. Plant Molecular Biology, 83, 433-443

Gao R, Wan Z Y, Wong S M. 2013. Plant growth retardationand conserved miRNAs are correlated to hibiscus chloroticringspot virus infection. PLOS ONE, 8, e85476.

Goodstal F J, Kohler G R, Randall L B, Bloom A J, Clair D AS. 2005. A major QTL introgressed from wild Lycopersiconhirsutum confers chilling tolerance to cultivated tomato(Lycopersicon esculentum). Theoretical and AppliedGenetics, 111, 898-905.

Guilfoyle T J, Ulmasov T, Hagen G. 1998. The ARF familyof transcription factors and their role in plant hormoneresponsivetranscription. Cell, 54, 619-627

Gutierrez L, Bussell J D, P?curara D I, Schwambacha J,P?curara M, Bellinia C. 2009. Phenotypic plasticity ofadventitious rooting in Arabidopsis is controlled by complexregulation of AUXIN RESPONSE FACTOR transcripts andmicroRNA abundance. The Plant Cell, 21, 3119-3132.

Ha M, Pang M X, Agarwal V, Chen Z J. 2008. Interspeciesregulation of microRNAs and their targets. Biochimica etBiophysica Acta, 1779, 735-742

Hanson P M, Sitathani K, Sadashiva A T, Yang R Y, GrahamE, Ledesma D. 2007. Performance of Solanum habrochaitesLA1777 introgression line hybrids for marketable tomato fruityield in Asia. Euphytica, 158, 167-178.

Itaya A, Bundschuh R, Archual A J, Joung J G, Fei Z J, Dai XB, Zhao P X, Tang Y H, Nelson R S, Ding B. 2008. SmallRNAs in tomato fruit and leaf development. Biochimica etBiophysica Acta, 1779, 99-107

Jin W B, Li F, Xiao L, Liang G W, Zhen Y X, Guo Z K, GuoA J. 2011. Microarray-based analysis of tomato miRNAregulated by Botrytis cinerea. Journal of Plant GrowthRegulation, 31, 38-46.

Jones J D, Dang J L. 2006. The plant immune system. Nature,444, 323-329

Jones-Rhoades M W, Bartel D P, Bartel B. 2006. MicroRNAsand their regulatory roles in plants. Annual Review of PlantBiology, 57,19-53.

Kim J H, Choi D, Kende H. 2003. The AtGRF family of putativetranscription factors is involved in leaf and cotyledon growthin Arabidopsis. The Plant Journal, 36, 94-104

Knauer S, Holt A, Rubio-Somoza I, Tucker E J, Hinze A, PischM, Javelle M, Timmermans M C, Tucker M R, Laux T.2013. A protodermal miR394 signal defines a region ofstem cell competence in the Arabidopsis shoot meristem.Development Cell, 24, 125-132.

Kozomara A, Griffiths-Jones S. 2011. miRBase: IntegratingmicroRNA annotation and deep-sequencing data. NucleicAcids Research, 39, D152-D157.

Labate J A, Grandillo S, Fulton T, Muños S, Caicedo A L, PeraltaI, Ji Y, Chetelat R T, Scott J, Gonzalo M J, Francis D, YangW, Knaap E V D, Baldo A M, Smith-White B, Mueller L A,Prince J P, Blanchard N E, Storey D B, Stevens M R, etal. 2007. Tomato. In: Kole C, ed., Genome Mapping andMolecular Breeding in Plants. Springer, Berlin, Heidelberg, New York. pp.1-125

Li F, Pignatta D, Bendix C, Brunkarda J O, Cohna M M, Tung J,Sun H Y, Kumarc P, Baker B 2012 MicroRNA regulation ofplant innate immune receptors. Proceedings of the NationalAcademy of Sciences of the United States of America, 109,1790-1795.

Liu H H, Tian X, Li Y J, Wu C A, Zheng C C. 2008.Microarray-based analysis of stress-regulated microRNAsin Arabidopsis thaliana. RNA, 14, 836-843

Lopez-Gomollon S, Mohorianu I, Szittya G, Moulton V, DalmayT. 2012. Diverse correlation patterns between microRNAsand their targets during tomato fruit development indicatesdifferent modes of microRNA actions. Planta, 236,1875-1887.

McDowell E T, Kapteyn J, Schmidt A, Li C, Kang J H, Descour A,Shi F, Larson M, Schilmiller A, An L L, Jones A D, PicherskyE, Soderlund C A, Gang D R. 2011. Comparative functionalgenomic analysis of solanum glandular trichome types.Plant Physiology, 55, 524-539

Meyers B C, Axtell M J, Bartel B, Bartel D P, Baulcombe D,Bowman J L, Cao X F, Carrington J C, Chen X M, Green P J,Griffiths-Jones S, Jacobsen S E, Mallory A C, Martienssen RA, Poethig R S, Qi Y J, Vaucheret H, Voinnet O, WatanabeY, Weigel D, Zhu J K. 2008. Criteria for annotation of plantMicroRNAs. The Plant Cell, 20, 3186-3190.

Mohorianu I, Schwach F, Runchun J, Lopez-Gomollon S, MoxonS, Szittya G, Sorefan K, Vincent M, Tamas D. 2011. Profilingof short RNAs during fleshy fruit development revealsstage-specific sRNAome expression patterns. The PlantJournal, 67, 232-246

Moxon S, Jing R, Szittya G, Schwach F, Rusholme P R L,Moulton V, Dalmay T. 2008. Deep sequencing of tomatoshort RNAs identifies microRNAs targeting genes involvedin fruit ripening. Genome Research, 18, 1602-1609.

Naqvi A R, Haq Q M, Mukherjee S K. 2010. MicroRNA profilingof tomato leaf curl new delhi virus (tolcndv) infected tomatoleaves indicates that deregulation of mir159/319 and mir172might be linked with leaf curl disease. Virology Journal, 7,1-16

Noda K I, Glover B J, Linstead P, Martin C. 1994. Flower colourintensity depends on specialized cell shape controlled bya Myb-related transcription factor. Nature, 369, 661-664.Palatnik J F, Allen E, Wu X L, Schommer C, SchwabR, Carrington J C, Weigel D. 2003. Control of leafmorphogenesis by microRNAs. Narure, 425, 257-263

Ranocha P, Chabannes M, Chamayou S, Danoun S, JauneauA, Boudet A , Goffner D. 2002. Laccase down-regulationcauses alterations in phenolic metabolism and cell wallstructure in poplar. Plant Physiology, 129, 145-155.

Rodriguez R E, Mecchia1 M A, Debernardi J M, SchommerC, Weigel D, Palatnik J F. 2010. Control of cell proliferationin Arabidopsis thaliana by microRNA miR396. Development,137, 103-112

Song J B, Gao S, Sun D, Li H, Shu X X, Yang Z M. 2013. miR394and LCR are involved in Arabidopsis salt and drought stressresponses in an abscisic acid-dependent manner. BMCPlant Biology,13, 210.

Spooner D M, Peralta I E, Knapp S. 2005. Comparison ofAFLPs with other markers for phylogenetic inference in wildtomatoes [Solanum L. section Lycopersicon (Mill.) Wettst.].TAXON, 54, 43-61.

Sunkar R, Zhou X F, Zheng Y, Zhang W X, Zhu J K. 2008.Identification of novel and candidate miRNAs in rice by highthroughput sequencing. BMC Plant Biology, 8, 25.

Sunkar R, Zhu J K. 2004. Novel and stress-regulatedMicroRNAs and other small rnas from arabidopsis. ThePlant Cell, 16, 2001-2019

Wang L, Mai Y X, Zhang Y C, Luo Q, Yang H Q. 2010.MicroRNA171c-targeted SCL6-II, SCL6-III, and SCL6-IVgenes regulate shoot branching in Arabidopsis. MolecularPlant, 3, 794-806.

Woo H R, Chung K M, Park J H, Oh S A, Ahn T, Hong S H,Jang S K, Nam H G. 2001. ORE9, an F-box protein thatregulates leaf senescence in Arabidopsis. The Plant Cell,13,1779-1790

Wu L, Zhang Q Q, Zhou H Y, Ni F R, Wu X Y, Qia Y J. 2009.Rice MicroRNA effector complexes and targets. The PlantCell, 21, 3421-3435.

Yan Y S, Chen X Y, Yang K, Sun Z X, Fu Y P, Zhang Y M,Fang R X. 2011. Overexpression of an F-box protein genereduces abiotic stress tolerance and promotes root growthin rice. Molecular Plant, 4, 190-197

Yin Z, Li C, Han X L, Shen F F. 2008. Identification of conservedmicroRNAs and their target genes in tomato (Lycopersiconesculentum). Gene, 414, 60- 66.

Yu G, Nguyen T T H, Guo Y X, Schauvinhold I, Auldridge ME, Bhuiyan N, Ben-Israel I, Iijima Y, Fridman E, Noel J P,Pichersky E. 2010. Enzymatic functions of wild tomatomethylketone synthases 1 and 2. Plant Physiology, 154,67-77.

Zhang J, Xu Y Y, Huan Q, Chong K. 2009. Deep sequencingof Brachypodium small RNAs at the global genome levelidentifies microRNAs involved in cold stress response. BMCGenomics, 10, 449.

Zheng X W, Zhu J H, Kapoor A, Zhu J K. 2007. Role ofArabidopsis AGO6 in siRNA accumulation, DNA methylationand transcriptional gene silencing. The EMBO Journal, 26,1691-1701

Zhu Q H, Spriggs A, Matthew L, Fan L J, Kennedy G, GublerF, Helliwell C. 2008. A diverse set of microRNAs andmicroRNA-like small RNAs in developing rice grains.Genome Research, 18, 1456-1465.
[1] DU Dan, HU Xin, SONG Xiao-mei, XIA Xiao-jiao, SUN Zhen-yu, LANG Min, PAN Yang-lu, ZHENG Yu, PAN Yu. SlTPP4 participates in ABA-mediated salt tolerance by enhancing root architecture in tomato[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2384-2396.
[2] TIAN Zhong-ling, ZHOU Jia-yan, ZHENG Jing-wu, HAN Shao-jie.

mgr-mir-9 implicates Meloidogyne graminicola infection in rice by targeting the effector MgPDI [J]. >Journal of Integrative Agriculture, 2023, 22(5): 1445-1454.

[3] LI Zheng-gang, NONG Yuan, Tahir FAROOQ, TANG Ya-fei, SHE Xiao-man, YU Lin, LAN Guo-bing, ZHOU Xue-ping, HE Zi-fu. Small RNA deep sequencing reveals the presence of multiple viral infections in cucurbit crops in Guangdong, China[J]. >Journal of Integrative Agriculture, 2022, 21(5): 1389-1400.
[4] YAN Xiao-xiao, LIU Xiang-yang, CUI Hong, ZHAO Ming-qin. The roles of microRNAs in regulating root formation and growth in plants[J]. >Journal of Integrative Agriculture, 2022, 21(4): 901-916.
[5] TANG Qiong, ZHENG Xiao-dong, GUO Jun, YU Ting. Tomato SlPti5 plays a regulative role in the plant immune response against Botrytis cinerea through modulation of ROS system and hormone pathways[J]. >Journal of Integrative Agriculture, 2022, 21(3): 697-709.
[6] SUN Yao-guang, HE Yu-qing, WANG He-xuan, JIANG Jing-bin, YANG Huan-huan, XU Xiang-yang. Genome-wide identification and expression analysis of GDSL esterase/lipase genes in tomato[J]. >Journal of Integrative Agriculture, 2022, 21(2): 389-406.
[7] ZHAO Juan, LIU Ting, LIU Wei-cheng, ZHANG Dian-peng, DONG Dan, WU Hui-ling, ZHANG Tao-tao, LIU De-wen. Transcriptomic insights into growth promotion effect of Trichoderma afroharzianum TM2-4 microbial agent on tomato plants[J]. >Journal of Integrative Agriculture, 2021, 20(5): 1266-1276.
[8] ZOU Zhong, GONG Wen-xiao, HUANG Kun, SUN Xiao-mei, JIN Mei-lin. Regulation of influenza virus infection by microRNAs[J]. >Journal of Integrative Agriculture, 2019, 18(7): 1421-1427.
[9] ZHANG Ya-ting, ZHANG Yu-qi, YANG Qi-chang, LI Tao. Overhead supplemental far-red light stimulates tomato growth under intra-canopy lighting with LEDs[J]. >Journal of Integrative Agriculture, 2019, 18(1): 62-69.
[10] FAN Xue-ying, LIN Wei-peng, LIU Rui, JIANG Ni-hao, CAI Kun-zheng. Physiological response and phenolic metabolism in tomato (Solanum lycopersicum) mediated by silicon under Ralstonia solanacearum infection[J]. >Journal of Integrative Agriculture, 2018, 17(10): 2160-2171.
[11] TANG Yun-jia, Johannes Liesche. The molecular mechanism of shade avoidance in crops- How data from Arabidopsis can help to identify targets for increasing yield and biomass production[J]. >Journal of Integrative Agriculture, 2017, 16(06): 1244-1255.
[12] YU Yun-qi, WU Qiong, SU Hua-nan, WANG Xue-feng, CAO Meng-ji, ZHOU Chang-yong . Small RNA deep sequencing reveals full-length genome of Citrus yellow vein clearing virus in Chongqing, China[J]. >Journal of Integrative Agriculture, 2017, 16(02): 503-508.
[13] BAI Miao, CHEN Wen-ting, XIE Bing-yan, YANG Guo-shun. A novel strategy to enhance resistance to Cucumber mosaic virus in tomato by grafting to transgenic rootstocks[J]. >Journal of Integrative Agriculture, 2016, 15(9): 2040-2048.
[14] WANG Li-bin, Jinhe Bai, YU Zhi-fang. Difference in volatile profile between pericarp tissue and locular gel in tomato fruit[J]. >Journal of Integrative Agriculture, 2016, 15(12): 2911-2920.
[15] LI Li, GUO Cheng, WANG Biao, ZHOU Tong, LEI Yang, DAI Yu-hua, HE Wen, LIANG Chun, WANG Xi-feng. RNAi-mediated transgenic rice resistance to Rice stripe virus[J]. >Journal of Integrative Agriculture, 2016, 15(11): 2539-2549.
No Suggested Reading articles found!