MicroRNAs in crop improvement: fine-tuners for complex traits

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Abstract

One of the most common challenges for both conventional and modern crop improvement is that the appearance of one desirable trait in a new crop variety is always balanced by the impairment of one or more other beneficial characteristics. The best way to overcome this problem is the flexible utilization of regulatory genes, especially genes that provide more efficient and precise regulation in a targeted manner. MicroRNAs (miRNAs), a type of short non-coding RNA, are promising candidates in this area due to their role as master modulators of gene expression at the post-transcriptional level, targeting messenger RNAs for cleavage or directing translational inhibition in eukaryotes. We herein highlight the current understanding of the biological role of miRNAs in orchestrating distinct agriculturally important traits by summarizing recent functional analyses of 65 miRNAs in 9 major crops worldwide. The integration of current miRNA knowledge with conventional and modern crop improvement strategies is also discussed.

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Figure 1: Distribution of miRNAs and their target genes.
Figure 2: Experimentally verified miRNA:trait relationships in rice.
Figure 3: Regulatory circuits orchestrated by miRNAs in rice.

References

  1. 1

    Takeda, S. & Matsuoka, M. Genetic approaches to crop improvement: responding to environmental and population changes. Nat. Rev. Genet. 9, 444–457 (2008).

  2. 2

    Brown, M. E. & Funk, C. C. Food security under climate change. Science 319, 580–581 (2008).

  3. 3

    Fedoroff, N. V. The past, present and future of crop genetic modification. New Biotechnol. 27, 461–465 (2010).

  4. 4

    Lombardo, L., Coppola, G. & Zelasco, S. New technologies for insect-resistant and herbicide-tolerant plants. Trends Biotechnol. 34, 49–57 (2016).

  5. 5

    Varshney, R. K., Hoisington, D. A. & Tyagi, A. K. Advances in cereal genomics and applications in crop breeding. Trends Biotechnol. 24, 490–499 (2006).

  6. 6

    Gratten, J. & Visscher, P. M. Genetic pleiotropy in complex traits and diseases: implications for genomic medicine. Genome Med. 8, 78 (2016).

  7. 7

    Voinnet, O. Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669–687 (2009).

  8. 8

    Chen, X. Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 25, 21–44 (2009).

  9. 9

    Sun, G. MicroRNAs and their diverse functions in plants. Plant Mol. Biol. 80, 17–36 (2012).

  10. 10

    Zhou, M. & Luo, H. MicroRNA-mediated gene regulation: potential applications for plant genetic engineering. Plant Mol. Biol. 83, 59–75 (2013).

  11. 11

    Zheng, L. L. & Qu, L. H. Application of microRNA gene resources in the improvement of agronomic traits in rice. Plant Biotechnol. J. 13, 329–336 (2015).

  12. 12

    Guan, X., Song, Q. & Chen, Z. J. Polyploidy and small RNA regulation of cotton fiber development. Trends Plant Sci. 19, 516–528 (2014).

  13. 13

    Jiao, Y. et al. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541–544 (2010).

  14. 14

    Wang, S. et al. Control of grain size, shape and quality by OsSPL16 in rice. Nat. Genet. 44, 950–954 (2012).

  15. 15

    Miura, K. et al. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545–549 (2010).

  16. 16

    Si, L. et al. OsSPL13 controls grain size in cultivated rice. Nat. Genet. 48, 447–456 (2016).

  17. 17

    Wang, L. et al. Coordinated regulation of vegetative and reproductive branching in rice. Proc. Natl Acad. Sci. USA 112, 15504–15509 (2015).

  18. 18

    Chuck, G., Cigan, A. M., Saeteurn, K. & Hake, S. The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat. Genet. 39, 544–549 (2007).

  19. 19

    Bhogale, S. et al. MicroRNA156: a potential graft-transmissible microRNA that modulates plant architecture and tuberization in Solanum tuberosum ssp. andigena. Plant Physiol. 164, 1011–1027 (2014).

  20. 20

    Chen, W. et al. Tuning LeSPL–CNR expression by SlymiR157 affects tomato fruit ripening. Sci. Rep. 5, 7852 (2015).

  21. 21

    Chuck, G., Whipple, C., Jackson, D. & Hake, S. The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137, 1243–1250 (2010).

  22. 22

    Ferreira e Silva, G. F. et al. microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development. Plant J. 78, 604–618 (2014).

  23. 23

    Zhang, X. et al. Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Lett. 585, 435–439 (2011).

  24. 24

    Huang, J., Li, Z. & Zhao, D. Deregulation of the osmiR160 target gene OsARF18 causes growth and developmental defects with an alteration of auxin signaling in rice. Sci. Rep. 6, 29938 (2016).

  25. 25

    Li, Y. et al. Multiple rice microRNAs are involved in immunity against the blast fungus Magnaporthe oryzae. Plant Physiol. 164, 1077–1092 (2014).

  26. 26

    Damodharan, S., Zhao, D. & Arazi, T. A common miRNA160-based mechanism regulates ovary patterning, floral organ abscission and lamina outgrowth in tomato. Plant J. 86, 458–471 (2016).

  27. 27

    Nizampatnam, N. R., Schreier, S. J., Damodaran, S., Adhikari, S. & Subramanian, S. microRNA160 dictates stage-specific auxin and cytokinin sensitivities and directs soybean nodule development. Plant J. 84, 140–153 (2015).

  28. 28

    Wang, Y. et al. MicroRNA167-directed regulation of the auxin response factors GmARF8a and GmARF8b is required for soybean nodulation and lateral root development. Plant Physiol. 168, 984–999 (2015).

  29. 29

    Liu, N. et al. Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. J. Exp. Bot. 65, 2507–2520 (2014).

  30. 30

    Zhu, Q. H., Upadhyaya, N. M., Gubler, F. & Helliwell, C. A. Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol. 9, 149 (2009).

  31. 31

    Lee, Y. S., Lee, D. Y., Cho, L. H. & An, G. Rice miR172 induces flowering by suppressing OsIDS1 and SNB, two AP2 genes that negatively regulate expression of Ehd1 and florigens. Rice 7, 31 (2014).

  32. 32

    Lauter, N., Kampani, A., Carlson, S., Goebel, M. & Moose, S. P. microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc. Natl Acad. Sci. USA 102, 9412–9417 (2005).

  33. 33

    Chuck, G., Meeley, R., Irish, E., Sakai, H. & Hake, S. The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1. Nat. Genet. 39, 1517–1521 (2007).

  34. 34

    Houston, K. et al. Variation in the interaction between alleles of HvAPETALA2 and microRNA172 determines the density of grains on the barley inflorescence. Proc. Natl Acad. Sci. USA 110, 16675–16680 (2013).

  35. 35

    Yan, Z. et al. miR172 regulates soybean nodulation. Mol. Plant Microbe Interact. 26, 1371–1377 (2013).

  36. 36

    Nair, S. K. et al. Cleistogamous flowering in barley arises from the suppression of microRNA-guided HvAP2 mRNA cleavage. Proc. Natl Acad. Sci. USA 107, 490–495 (2010).

  37. 37

    Martin, A. et al. Graft-transmissible induction of potato tuberization by the microRNA miR172. Development 136, 2873–2881 (2009).

  38. 38

    Yang, C. et al. Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Environ. 36, 2207–2218 (2013).

  39. 39

    Ori, N. et al. Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat. Genet. 39, 787–791 (2007).

  40. 40

    Zhang, C. et al. Suppression of jasmonic acid-mediated defense by viral-inducible microRNA319 facilitates virus infection in rice. Mol. Plant 9, 1302–1314 (2016).

  41. 41

    Zhao, W. et al. Identification of jasmonic acid-associated microRNAs and characterization of the regulatory roles of the miR319/TCP4 module under root-knot nematode stress in tomato. J. Exp. Bot. 66, 4653–4667 (2015).

  42. 42

    Tsuji, H. et al. GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J. 47, 427–444 (2006).

  43. 43

    Wang, Y. et al. TamiR159 directed wheat TaGAMYB cleavage and its involvement in anther development and heat response. PLoS ONE 7, e48445 (2012).

  44. 44

    Guan, X. et al. miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nat. Commun. 5, 3050 (2014).

  45. 45

    Li, J. et al. miRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). BMC Plant Biol. 12, 220 (2012).

  46. 46

    Berger, Y. et al. The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136, 823–832 (2009).

  47. 47

    Fang, Y., Xie, K. & Xiong, L. Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice. J. Exp. Bot. 65, 2119–2135 (2014).

  48. 48

    Feng, H. et al. The target gene of tae-miR164, a novel NAC transcription factor from the NAM subfamily, negatively regulates resistance of wheat to stripe rust. Mol. Plant Pathol. 15, 284–296 (2014).

  49. 49

    Che, R. et al. Control of grain size and rice yield by GL2-mediated brassinosteroid responses. Nat. Plants 2, 15195 (2015).

  50. 50

    Duan, P. et al. Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nat. Plants 2, 15203 (2015).

  51. 51

    Gao, F. et al. Blocking miR396 increases rice yield by shaping inflorescence architecture. Nat. Plants 2, 15196 (2015).

  52. 52

    Liu, H. et al. OsmiR396d-regulated OsGRFs function in floral organogenesis in rice through binding to their targets OsJMJ706 and OsCR4. Plant Physiol. 165, 160–174 (2014).

  53. 53

    Hu, J. et al. A rare allele of GS2 enhances grain size and grain yield in rice. Mol. Plant 8, 1455–1465 (2015).

  54. 54

    Hewezi, T., Maier, T. R., Nettleton, D. & Baum, T. J. The Arabidopsis microRNA396-GRF1/GRF3 regulatory module acts as a developmental regulator in the reprogramming of root cells during cyst nematode infection. Plant Physiol. 159, 321–335 (2012).

  55. 55

    Guo, S. et al. The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat. Commun. 4, 1566 (2013).

  56. 56

    Yan, Y., Wang, H., Hamera, S., Chen, X. & Fang, R. miR444a has multiple functions in the rice nitrate-signaling pathway. Plant J. 78, 44–55 (2014).

  57. 57

    Wang, H. et al. A signaling cascade from miR444 to RDR1 in rice antiviral RNA silencing pathway. Plant Physiol. 170, 2365–2377 (2016).

  58. 58

    Iwamoto, M. & Tagiri, A. MicroRNA-targeted transcription factor gene RDD1 promotes nutrient ion uptake and accumulation in rice. Plant J. 85, 466–477 (2016).

  59. 59

    Curaba, J., Talbot, M., Li, Z. Y. & Helliwell, C. Over-expression of microRNA171 affects phase transitions and floral meristem determinancy in barley. BMC Plant Biol. 13, 6 (2013).

  60. 60

    Gao, S. et al. A cotton miRNA is involved in regulation of plant response to salt stress. Sci. Rep. 6, 19736 (2016).

  61. 61

    Zhao, X. Y. et al. The tae-miR408-mediated control of TaTOC1 genes transcription is required for the regulation of heading time in wheat. Plant Physiol. 170, 1578–1594 (2016).

  62. 62

    Juarez, M. T., Kui, J. S., Thomas, J., Heller, B. A. & Timmermans, M. C. P. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428, 84–88 (2004).

  63. 63

    Tang, J. et al. Semi-dominant mutations in the CC-NB-LRR-type R gene, NLS1, lead to constitutive activation of defense responses in rice. Plant J. 66, 996–1007 (2011).

  64. 64

    de Vries, S., Kloesges, T. & Rose, L. E. Evolutionarily dynamic, but robust, targeting of resistance genes by the miR482/2118 gene family in the Solanaceae. Genome Biol. Evol. 7, 3307–3321 (2015).

  65. 65

    Li, F. et al. MicroRNA regulation of plant innate immune receptors. Proc. Natl Acad. Sci. USA 109, 1790–1795 (2012).

  66. 66

    Shivaprasad, P. V. et al. A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24, 859–874 (2012).

  67. 67

    Zhu, Q. H. et al. miR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton. PLoS ONE 8, e84390 (2013).

  68. 68

    Ouyang, S. Q. et al. MicroRNAs suppress NB domain genes in tomato that confer resistance to Fusarium oxysporum. PLoS Pathog. 10, e1004464 (2014).

  69. 69

    Yang, L. et al. Overexpression of potato miR482e enhanced plant sensitivity to Verticillium dahliae infection. J. Integr. Plant Biol. 57, 1078–1088 (2015).

  70. 70

    Wei, C., Kuang, H., Li, F. & Chen, J. The I2 resistance gene homologues in Solanum have complex evolutionary patterns and are targeted by miRNAs. BMC Genomics 15, 743 (2014).

  71. 71

    Liu, J. et al. The miR9863 family regulates distinct Mla alleles in barley to attenuate NLR receptor-triggered disease resistance and cell-death signaling. PLoS Genet. 10, e1004755 (2014).

  72. 72

    Zhang, T. et al. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants 2, 16153 (2016).

  73. 73

    Weiberg, A. et al. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342, 118–123 (2013).

  74. 74

    Fan, Y. et al. PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc. Natl Acad. Sci. USA 13, 15144–15149 (2016).

  75. 75

    Zhang, Y. C. et al. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat. Biotechnol. 31, 848–852 (2013).

  76. 76

    Li, X. et al. MicroRNA393 is involved in nitrogen-promoted rice tillering through regulation of auxin signal transduction in axillary buds. Sci. Rep. 6, 32158 (2016).

  77. 77

    Xia, K. et al. OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS ONE 7, e30039 (2012).

  78. 78

    Yang, J. H., Han, S. J., Yoon, E. K. & Lee, W. S. ‘Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells’. Nucleic Acids Res. 34, 1892–1899 (2006).

  79. 79

    Bian, H. et al. Distinctive expression patterns and roles of the miRNA393/TIR1 homolog module in regulating flag leaf inclination and primary and crown root growth in rice (Oryza sativa). New Phytol. 196, 149–161 (2012).

  80. 80

    Hu, B. et al. LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol. 156, 1101–1115 (2011).

  81. 81

    Hu, B. et al. microRNA399 is involved in multiple nutrient responses in rice. Front. Plant Sci. 6, 188 (2015).

  82. 82

    Lin, S. I. et al. Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol. 51, 2119–2131 (2010).

  83. 83

    Guo, H. S., Xie, Q., Fei, J. F. & Chua, N. H. MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17, 1376–1386 (2005).

  84. 84

    Allen, E., Xie, Z., Gustafson, A. M. & Carrington, J. C. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207–221 (2005).

  85. 85

    Cuperus, J. T., Fahlgren, N. & Carrington, J. C. Evolution and functional diversification of MIRNA genes. Plant Cell 23, 431–442 (2011).

  86. 86

    Wu, J. et al. Viral-inducible Argonaute18 confers broad-spectrum virus resistance in rice by sequestering a host microRNA. eLife 4, e05733 (2015).

  87. 87

    Varallyay, E., Valoczi, A., Agyi, A., Burgyan, J. & Havelda, Z. Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO J. 29, 3507–3519 (2010).

  88. 88

    Xian, Z. et al. miR168 influences phase transition, leaf epinasty, and fruit development via SlAGO1s in tomato. J. Exp. Bot. 65, 6655–6666 (2014).

  89. 89

    Xu, W., Meng, Y. & Wise, R. P. Mla- and Rom1-mediated control of microRNA398 and chloroplast copper/zinc superoxide dismutase regulates cell death in response to the barley powdery mildew fungus. New Phytol. 201, 1396–412 (2014).

  90. 90

    Zhang, X. et al. Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol. Lett. 33, 403–409 (2011).

  91. 91

    Li, W. X. et al. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20, 2238–2251 (2008).

  92. 92

    Budak, H. & Akpinar, B. A. Plant miRNAs: biogenesis, organization and origins. Funct. Integr. Genomics 15, 523–531 (2015).

  93. 93

    Nozawa, M., Miura, S. & Nei, M. Origins and evolution of microRNA genes in plant species. Genome Biol. Evol. 4, 230–239 (2012).

  94. 94

    Taylor, R. S., Tarver, J. E., Hiscock, S. J. & Donoghue, P. C. Evolutionary history of plant microRNAs. Trends Plant Sci. 19, 175–182 (2014).

  95. 95

    Campo, S. et al. Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytol. 199, 212–227 (2013).

  96. 96

    Franco-Zorrilla, J. M. et al. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39, 1033–1037 (2007).

  97. 97

    Niu, Q. W. et al. Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat. Biotechnol. 24, 1420–1428 (2006).

  98. 98

    Liu, Q. & Chen, Y. Q. The potential roles of microRNAs in molecular breeding. Methods Mol. Biol. 877, 303–311 (2012).

  99. 99

    Liu, Q., Wang, H., Hu, H. & Zhang, H. Genome-wide identification and evolutionary analysis of positively selected miRNA genes in domesticated rice. Mol. Genet. Genomics 290, 593–602 (2015).

  100. 100

    Liu, T. et al. Global investigation of the co-evolution of MIRNA genes and microRNA targets during soybean domestication. Plant J. 85, 396–409 (2016).

  101. 101

    Wang, C. M. et al. Loop nucleotide polymorphism in a putative miRNA precursor associated with seed length in rice (Oryza sativa L.). Int. J. Biol. Sci. 9, 578–586 (2013).

  102. 102

    Zhao, M. et al. Regulation of OsmiR156h through alternative polyadenylation improves grain yield in rice. PLoS ONE 10, e0126154 (2015).

  103. 103

    Zhao, P. et al. Investigating the molecular genetic basis of heterosis for internode expansion in maize by microRNA transcriptomic deep sequencing. Funct. Integr. Genomics 15, 261–270 (2015).

  104. 104

    Li, A. L. et al. mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant Cell 26, 1878–1900 (2014).

  105. 105

    Fang, R., Li, L. & Li, J. Spatial and temporal expression modes of MicroRNAs in an elite rice hybrid and its parental lines. Planta 238, 259–269 (2013).

  106. 106

    Shivaprasad, P. V., Dunn, R. M., Santos, B. A., Bassett, A. & Baulcombe, D. C. Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J. 31, 257–266 (2012).

  107. 107

    Shen, Y. et al. Cytoplasmic male sterility-regulated novel microRNAs from maize. Funct. Integr. Genomics 11, 179–191 (2011).

  108. 108

    Yan, J., Zhang, H., Zheng, Y. & Ding, Y. Comparative expression profiling of miRNAs between the cytoplasmic male sterile line MeixiangA and its maintainer line MeixiangB during rice anther development. Planta 241, 109–123 (2015).

  109. 109

    Shan, Q. et al. Targeted genome modification of crop plants using a CRISPR-Cas system. Nat. Biotechnol. 31, 686–688 (2013).

  110. 110

    Li, J., Sun, Y., Du, J., Zhao, Y. & Xia, L. Generation of targeted point mutations in rice by a modified CRISPR/Cas9 system. Mol. Plant 10, 526–529 (2017).

  111. 111

    Barrangou, R. et al. Advances in CRISPR-Cas9 genome engineering: lessons learned from RNA interference. Nucleic Acids Res. 43, 3407–3419 (2015).

  112. 112

    Li, J. et al. Gene replacements and insertions in rice by intron targeting using CRISPR–Cas9. Nat. Plants 2, 16139 (2016).

  113. 113

    Zong, Y. et al. Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat. Biotechnol. 35, 438–440 (2017).

  114. 114

    Lu, Y. & Zhu, J. K. Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol. Plant 10, 523–525 (2017).

  115. 115

    Fukuoka, S. et al. Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325, 998–1001 (2009).

  116. 116

    Tian, C., Zuo, Z. & Qiu, J. L. Identification and characterization of ABA-responsive microRNAs in rice. J. Genet. Genomics 42, 393–402 (2015).

  117. 117

    Du, H. et al. A GH3 family member, OsGH3–2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. J. Exp. Bot. 63, 6467–6480 (2012).

  118. 118

    Ding, Y., Ye, Y., Jiang, Z., Wang, Y. & Zhu, C. MicroRNA390 is involved in cadmium tolerance and accumulation in rice. Front. Plant Sci. 7, 235 (2016).

  119. 119

    Yuan, N. et al. Heterologous expression of a rice miR395 gene in Nicotiana tabacum impairs sulfate homeostasis. Sci. Rep. 6, 28791 (2016).

  120. 120

    Wu, J. G. et al. ROS accumulation and antiviral defence control by microRNA528 in rice. Nat. Plants 3, 16203 (2017).

  121. 121

    Nosaka, M. et al. Role of transposon-derived small RNAs in the interplay between genomes and parasitic DNA in rice. PLoS Genet. 8, e1002953 (2012).

  122. 122

    Xia, K. et al. Rice microRNA osa-miR1848 targets the obtusifoliol 14a-demethylase gene OsCYP51G3 and mediates the biosynthesis of phytosterols and brassinosteroids during development and in response to stress. New Phytol. 208, 790–802 (2015).

  123. 123

    Xia, K. et al. OsWS1 involved in cuticular wax biosynthesis is regulated by osa-miR1848. Plant Cell Environ. 38, 2662–2673 (2015).

  124. 124

    Feng, H. et al. Monodehydroascorbate reductase gene, regulated by the wheat PN-2013 miRNA, contributes to adult wheat plant resistance to stripe rust through ROS metabolism. Biochim. Biophys. Acta 1839, 1–12 (2014).

  125. 125

    Feng, H. et al. Target of tae-miR408, a chemocyanin-like protein gene (TaCLP1), plays positive roles in wheat response to high-salinity, heavy cupric stress and stripe rust. Plant Mol. Biol. 83, 433–443 (2013).

  126. 126

    Buxdorf, K. et al. Identification and characterization of a novel miR159 target not related to MYB in tomato. Planta 232, 1009–1022 (2010).

  127. 127

    Jia, X. et al. Small tandem target mimic-mediated blockage of microRNA858 induces anthocyanin accumulation in tomato. Planta 242, 283–293 (2015).

  128. 128

    Wang, Y. et al. Function and evolution of a microRNA that regulates a Ca2+-ATPase and triggers the formation of phased small interfering RNAs in tomato reproductive growth. Plant Cell 23, 3185–3203 (2011).

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Acknowledgements

This work was supported by the grants from the Chinese Academy of Sciences (XDA08010400), the National Key Research and Development Program of China (2016YFD0101801), and the National Natural Science Foundation of China (31571248 and 31201182). We apologize to our colleagues whose work was not included or sufficiently discussed in this article because of space restrictions.

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J.T. and C.C. wrote this article.

Correspondence to Jiuyou Tang or Chengcai Chu.

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Tang, J., Chu, C. MicroRNAs in crop improvement: fine-tuners for complex traits. Nature Plants 3, 17077 (2017) doi:10.1038/nplants.2017.77

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