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Review
. 2021 Aug 18;1(1):6.
doi: 10.1007/s44154-021-00005-2.

Roles of small RNAs in crop disease resistance

Jun Tang #  1   2 , Xueting Gu #  1   2 , Junzhong Liu  3 , Zuhua He  4
Affiliations
Review

Roles of small RNAs in crop disease resistance

Jun Tang et al. Stress Biol. .

Abstract

Small RNAs (sRNAs) are a class of short, non-coding regulatory RNAs that have emerged as critical components of defense regulatory networks across plant kingdoms. Many sRNA-based technologies, such as host-induced gene silencing (HIGS), spray-induced gene silencing (SIGS), virus-induced gene silencing (VIGS), artificial microRNA (amiRNA) and synthetic trans-acting siRNA (syn-tasiRNA)-mediated RNA interference (RNAi), have been developed as disease control strategies in both monocot and dicot plants, particularly in crops. This review aims to highlight our current understanding of the roles of sRNAs including miRNAs, heterochromatic siRNAs (hc-siRNAs), phased, secondary siRNAs (phasiRNAs) and natural antisense siRNAs (nat-siRNAs) in disease resistance, and sRNAs-mediated trade-offs between defense and growth in crops. In particular, we focus on the diverse functions of sRNAs in defense responses to bacterial and fungal pathogens, oomycete and virus in crops. Further, we highlight the application of sRNA-based technologies in protecting crops from pathogens. Further research perspectives are proposed to develop new sRNAs-based efficient strategies to breed non-genetically modified (GMO), disease-tolerant crops for sustainable agriculture.

Keywords: Crop diseases; HIGS; RNAi; RNAi-based technology; Small RNAs.

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Conflict of interest statement

Author Z.H. is a member of the Editorial Board and was not involved in the journal's review of, or decisions related to, this manuscript.

Figures

Fig. 1
Fig. 1
Small RNAs regulate plant defense against-pathogen. In response to pathogen attacks, plants accurately fine-tune the expression of endogenous gene through sRNAs-trigged mRNA cleavage, translational repression as well as DNA methylation. a sRNAs regulate plant resistance to various pathogens through mRNA cleavage or translational repression. miR164 (Wang et al. 2018), miR167 (Zhao et al. 2020) and miR169 (Li et al. 2017) which directly target transcription factors play negative roles in plant response to M. oryzae while miR166 (Salvador-Guirao et al. 2018) and miR398 (Li et al. 2019a) are positive regulators. miR160 (Natarajan et al. 2018) and miR393 (Wong et al. 2014) regulate the interactions between crop and oomycetes. Some other small RNAs such as miR156 (Liu et al. 2019) and miR159 (Zhao et al. 2015b) modulate the disease resistance against bacterial pathogens. Upon virus infection, some miRNAs target essential components of RNAi to regulate plant immunity, like miR168 (Du et al. 2011). b Hc-siRNA-mediated DNA methylation at the MITE region of PigmS promoter represses PigmS expression (Deng et al. 2017). c Plant small RNAs not only function in host cells, but also move into invasive enemies. For example, miR159, miR166 (Zhang et al. 2016c) and miR1023 (Jiao and Peng 2018) trigger the silencing of fungal virulence genes. d PhasiRNA pathway fine-tunes the expression level of R gene in the absence of pathogen (González et al. 2015). e During the long-term arm-race between crops and pathogens, pathogens can secrete specific proteins or small RNAs into plant cells to enhance plant susceptibility to ensure their own virulence. For instance, B. cinerea delivers Bc-siRNAs to plant cell to hijack host RNAi pathway (Weiberg et al. 2013). TAL-effectors such as Tal9a from genus Xanthomonas can bind to host specific promoter motifs and activate host genes expression (Moscou and Bogdanove 2009). A non-TAL effector XopQ can up-regulates host sRNAmiR1876 through an unknown mechanism (Jiang et al. 2020). Some proteins such as PSR1 and PSR2 (Xiong et al. 2014) from P. sojae and P19 (Silhavy et al. 2002), P0 (Li et al. 2019b) , CP (Karran and Sanfaçon 2014), RNase 3 (Cuellar et al. ; Kreuze et al. 2005), C2 (Yang et al. 2013) from different kinds of viruses can disrupt host immune response by suppressing RNA silencing pathways in plants
Fig. 2
Fig. 2
sRNA-based technologies in protecting crop plants. Many sRNA-based technologies have been developed to protect plants from pathogens. a Artificial microRNA (amiRNA) approach. For example, the transgenic barley lines that carry a polycistronic amiRNA precursor construct (VirusBuster171) expressing three amiRNAs simultaneously under the control of a constitutive promoter, display enhanced resistance to Wheat dwarf virus (WDV) (Kis et al. 2016). b Short tandem target mimic (STTM) approach in modulating the activity of miRNAs. STTM is composed of two miRNA binding sites which have mismatches at the mRNA cleavage sites. The two mimic sequences are usually separated by a spacer linker. In soybean, inhibition of miR1507 as well as miR482 by STTM compromises their suppression of NBS-LRR genes (Bao et al. 2018). c Synthetic trans-acting siRNA approach. MiRNAs target TAS loci and produce phased, secondary siRNAs with the help of DCL4. Thus, TAS genes are engineered to express multiple synthetic ta-siRNAs (syn-tasiRNAs) that target multiple viruses at diverse genomic position. d Host-induced gene silencing (HIGS), spray-induced gene silencing (SIGS) and virus-induced gene silencing (VIGS). Based on that plant sRNAs can be transferred to organisms colonizing or feeding on the plant, scientists engineer transgenic plants which produce sRNAs targeting pathogen sequences to avoid infection. Meanwhile, VIGS, which use the virus expression vector as the medium, and SIGS, which directly use pathogen-gene-targeting dsRNAs or sRNAs, are two other strategies. These new approaches not only control plant disease but also have the advantages of simplicity, high specificity, flexibility and stability
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