Abstract
Argonaute proteins are key players in small RNA-guided gene-silencing, which plays an important role in plant stress tolerance. However, little is known about how Argonaute genes affect the water-use efficiency (WUE) of apple (Malus domestica) or its responses to different abiotic stresses. We identified and characterized MdAGOs in apple and analyzed their chromosome locations, exon/intron structures, phylogeny, and the distribution of conserved motifs. We also examined the expression profiling of responses to abiotic stress and conducted molecular cloning of MdAGO4.1. In all, 16 MdAGOs were identified and characterized, then grouped into three separate clusters. Our qRT-PCR data demonstrated that these genes are induced by drought, salt, cold, and ABA treatments, indicating that they are good candidates for further analysis of their activities and functions. We have previously shown that, during long-term moderate drought, the abundance of MdAGO4.1 protein is increased in ‘Qinguan’ apple (a cultivar with high WUE) leaves, but not in ‘Naganofuji No. 2’. These changes are in accordance with alterations in their WUE and expression of MdAGO4.1 under the same test conditions as those used in the current study. Therefore, MdAGO4.1 is a putative gene that positively regulates WUE. Our findings provide evidence that MdAGOs have a role in plant adaptations to abiotic stress and can be exploited to improve WUE. These results will serve as a framework for future functional studies of that gene family in apple.
Similar content being viewed by others
Abbreviations
- ABA:
-
Abscisic acid
- ABRE:
-
Abscisic acid response element
- AGO:
-
Argonaute
- EST:
-
Expressed sequence tag
- HSE:
-
Heat shock element
- LTR:
-
Low-temperature-responsive element
- MBS:
-
MYB binding site
- MdAGO:
-
Argonaute of apple
- miRNA:
-
MicroRNA
- ORF:
-
Open reading frame
- qRT-PCR:
-
Quantitative real-time PCR
- siRNA:
-
Short interfering RNAs
- WUE:
-
Water-use efficiency
- MeJA:
-
Methyl jasmonate
- GA:
-
Gibberellic acid
References
Bai M, Yang G, Chen W et al (2012) Genome-wide identification of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families and their expression analyses in response to viral infection and abiotic stresses in Solanum lycopersicum. Gene 501:52–62
Bassett CL (2013) Water use and drought response in cultivated and wild apples. In: Vahdati K, Leslie C (eds) Agricultural and biological sciences, vol 8. Alpha Science International Ltd, UK, pp 249–275
Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795
Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116
Drinnenberg IA, Weinberg DE, Xie KT et al (2009) RNAi in budding yeast. Science 326:544–550
Du JL, Zhang SW, Huang HW et al (2015) The splicing factor PRP31 is involved in transcriptional gene silencing and stress response in Arabidopsis. Mol Plant 8:1053–1068
Gunter M (2013) Argonaute proteins: functional insights and emerging roles. Nat Rev 14:447–459
He J, Gray J, Leisner S (2010) A Pelargonium Argonaute4 gene shows organ-specific expression and differences in RNA and protein levels. J Plant Physiol 167:319–325
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300
Hobo T, Asada M, Kowyama Y, Hattori T (1999) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19:679–689
Hock J, Meister G (2008) The Argonaute protein family. Genome Biol 9:210
Hutvagner G, Simard MJ (2008) Argonaute proteins: key players in RNA silencing. Nat Rev Mol Cell Biol 9:22–32
Jiang C, Iu B, Singh J (1996) Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant Mol Biol 30:679–684
Jinek M, Doudna JA (2009) A three-dimensional view of the molecular machinery of RNA interference. Nature 457:405–412
Kapoor M, Arora R, Lama T et al (2008) Genome-wide identification, organization and phylogenetic analysis of Dicer-like, Argonaute and RNA dependent RNA Polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genom 9:451
Lescot M, Déhais P, Moreau Y et al (2002) PlantCARE: a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Li W, Cui X, Meng Z et al (2012) Transcriptional regulation of Arabidopsis MIR168a and ARGONAUTE1 homeostasis in abscisic acid and abiotic stress responses. Plant Physiol 158:1279–1292
Liu R, Meng J (2003) MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Yi Chuan 25:317–321
Liu B, Cheng L, Ma F et al (2012) Growth, biomass allocation, and water use efficiency of 31 apple cultivars grown under two water regimes. Agrofor Syst 84:117–129
Meister G (2013) Argonaute proteins: functional insights and emerging roles. Nat Rev Genet 14:447–459
Meng F, Jia H, Ling N et al (2013) Cloning and characterization of two Argonaute genes in wheat (Triticum aestivum L.). BMC Plant Biol 13:18
Qi Y, He X, Wang X et al (2006) Distinct catalytic and non-catalytic roles of Argonaute4 in RNA-directed DNA methylation. Nature 443:1008–1012
Rieping M, Schoffl F (1992) Synergistic effect of upstream sequences, CCAAT box elements, and HSE sequences for enhanced expression of chimaeric heat shock genes in transgenic tobacco. Mol Gen Genet 231:226–232
Shao Y, Qin Y, Zou Y, Ma F (2014) Genome-wide identification and expression profiling of the SnRK2 gene family in Malus prunifolia. Gene 552:87–97
Simon B, Kirkpatrick JP, Eckhardt S et al (2011) Recognition of 2′-O-methylated 3′-end of piRNA by the PAZ domain of a Piwi protein. Structure 19:172–180
Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tan Y, Wang S, Liang D et al (2014) Genome-wide identification and expression profiling of the cystatin gene family in apple (Malus domestica Borkh.). Plant Physiol Biochem 79:88–97
Velasco R, Zharkikh A, Affourtit J et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839
Wang B, Duan CG, Wang X et al (2015) HOS1 regulates Argonaute1 by promoting transcription of the microRNA gene MIR168b in Arabidopsis. Plant J 81:861–870
Xiong LM, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell Suppl 14:165–183
Ye R, Wang W, Iki T et al (2012) Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Mol Cell 46:859–870
Zhao T, Liang D, Wang P et al (2012) Genome-wide analysis and expression profiling of the DREB transcription factor gene family in Malus under abiotic stress. Mol Genet Genom 287:423–436
Zhao H, Zhao K, Wang J et al (2015) Comprehensive analysis of Dicer-Like, Argonaute, and RNA-dependent RNA polymerase gene families in grapevine (Vitis vinifera). J Plant Growth Regul 34:108–121
Zhou S, Li M, Guan Q et al (2015) Photosynthesis system plays main roles for high water-use efficiency under drought stress in Malus proved by physiological and proteome analysis. Plant Sci 236:44–60
Acknowledgments
This work was supported by the State Key Program of the National Natural Science Foundation of China (31330068), the Key Program of the State Key Laboratory of Crop Stress Biology for Arid Areas (CSBAAZD1302), and the earmarked fund for the China Agriculture Research System (CARS-28). The authors are grateful to Priscilla Licht for help in revising our English composition and Mr. Zhengwei Ma for management of the apple trees.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This research had no potential conflicts of interest and did not involve any human participants or animals.
Additional information
Communicated by M Hajduch.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhou, S., Ma, S., Li, M. et al. Comprehensive genomic analysis and expression profiling of Argonaute gene family and examination of their regulatory roles in water-use efficiency and abiotic stress responses in apple. Acta Physiol Plant 38, 231 (2016). https://doi.org/10.1007/s11738-016-2245-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-016-2245-0