Featured Publications

Phased Secondary Small Interfering RNAs (phasiRNAs) in Plants: Their Biogenesis, Genic Sources, and Roles in Stress Responses, Development, and Reproduction

Liu, Y, Teng, C, Xia, R, Meyers, BC
Plant Cell. 20120. doi: 10.1105/tpc.20.00335.

Abstract
PhasiRNAs (phased, secondary, small interfering RNAs) constitute a major category of small RNAs (sRNAs) in plants, but most of their functions are still poorly defined. Some phasiRNAs, known as trans-acting small interfering RNAs (tasiRNAs), are known to target complementary mRNAs for degradation and to function in development. Yet for other phasiRNAs, either the targets or biological roles remain speculative. New insights into phasiRNA biogenesis, their conservation, and variation across the flowering plants continue to emerge via the increased availability of plant genomic sequences, deeper and more sophisticated sequencing approaches, and improvements in computational biology and biochemical/molecular/genetic analyses. In this review, we survey recent progress in phasiRNA biology, in particular focusing on two classes associated with male reproduction: 21-nt (accumulated early in anther ontogeny) and 24-nt (produced in somatic cells during meiosis) phasiRNAs. We describe phasiRNA biogenesis, function, and evolution, and define the unanswered questions that represent topics for future research.

Quantitative, super-resolution localization of small RNAs with sRNA-PAINT

Huang, K, Demirci, F, Batish, M, Treible, W, Meyers, BC, Caplan, JL et al..
Nucleic Acids Res. 2020. doi: 10.1093/nar/gkaa623.

Abstract
Small RNAs are non-coding RNAs that play important roles in the lives of both animals and plants. They are 21- to 24-nt in length and ∼10 nm in size. Their small size and high diversity have made it challenging to develop detection methods that have sufficient resolution and specificity to multiplex and quantify. We created a method, sRNA-PAINT, for the detection of small RNAs with 20 nm resolution by combining the super-resolution method, DNA-based points accumulation in nanoscale topography (DNA-PAINT), and the specificity of locked nucleic acid (LNA) probes for the in situ detection of multiple small RNAs. The method relies on designing probes to target small RNAs that combine DNA oligonucleotides (oligos) for PAINT with LNA-containing oligos for hybridization; therefore, we developed an online tool called ‘Vetting & Analysis of RNA for in situ Hybridization probes’ (VARNISH) for probe design. Our method utilizes advances in DNA-PAINT methodologies, including qPAINT for quantification, and Exchange-PAINT for multiplexing. We demonstrated these capabilities of sRNA-PAINT by detecting and quantifying small RNAs in different cell layers of early developmental stage maize anthers that are important for male sexual reproduction.

sRNA-FISH: versatile fluorescent in situ detection of small RNAs in plants

Huang, K, Baldrich, P, Meyers, BC, Caplan, JL
Plant J. 2019;98 (2):359-369. doi: 10.1111/tpj.14210.

Abstract
Localization of mRNA and small RNAs (sRNAs) is important for understanding their function. Fluorescent in situ hybridization (FISH) has been used extensively in animal systems to study the localization and expression of sRNAs. However, current methods for fluorescent in situ detection of sRNA in plant tissues are less developed. Here we report a protocol (sRNA-FISH) for efficient fluorescent detection of sRNAs in plants. This protocol is suitable for application in diverse plant species and tissue types. The use of locked nucleic acid probes and antibodies conjugated with different fluorophores allows the detection of two sRNAs in the same sample. Using this method, we have successfully detected the co-localization of miR2275 and a 24-nucleotide phased small interfering RNA in maize anther tapetal and archesporial cells. We describe how to overcome the common problem of the wide range of autofluorescence in embedded plant tissue using linear spectral unmixing on a laser scanning confocal microscope. For highly autofluorescent samples, we show that multi-photon fluorescence excitation microscopy can be used to separate the target sRNA-FISH signal from background autofluorescence. In contrast to colorimetric in situ hybridization, sRNA-FISH signals can be imaged using super-resolution microscopy to examine the subcellular localization of sRNAs. We detected maize miR2275 by super-resolution structured illumination microscopy and direct stochastic optical reconstruction microscopy. In this study, we describe how we overcame the challenges of adapting FISH for imaging in plant tissue and provide a step-by-step sRNA-FISH protocol for studying sRNAs at the cellular and even subcellular level.

24-nt reproductive phasiRNAs are broadly present in angiosperms

Xia, R, Chen, C, Pokhrel, S, Ma, W, Huang, K, Patel, P et al.
Nat Commun. 2019;10
(1):627. doi: 
10.1038/s41467-019-08543-0.

Abstract
Small RNAs are key regulators in plant growth and development. One subclass, phased siRNAs (phasiRNAs) require a trigger microRNA for their biogenesis. In grasses, two pathways yield abundant phasiRNAs during anther development; miR2275 triggers one class, 24-nt phasiRNAs, coincident with meiosis, while a second class of 21-nt phasiRNAs are present in premeiotic anthers. Here we report that the 24-nt phasiRNA pathway is widely present in flowering plants, indicating that 24-nt reproductive phasiRNAs likely originated with the evolutionary emergence of anthers. Deep comparative genomic analyses demonstrated that this miR2275/24-nt phasiRNA pathway is widely present in eudicots plants, however, it is absent in legumes and in the model plant Arabidopsis, demonstrating a dynamic evolutionary history of this pathway. In Solanaceae species, 24-nt phasiRNAs were observed, but the miR2275 trigger is missing and some loci displaying 12-nt phasing. Both the miR2275-triggered and Solanaceae 24-nt phasiRNAs are enriched in meiotic stages, implicating these phasiRNAs in anther and/or pollen development, a spatiotemporal pattern consistent in all angiosperm lineages that deploy them.

Plant Extracellular Vesicles Contain Diverse Small RNA Species and Are Enriched in 10- to 17-Nucleotide "Tiny" RNAs

Baldrich, P, Rutter, BD, Karimi, HZ, Podicheti, R, Meyers, BC, Innes, RW et al.
Plant Cell. 2019;31 (2):315-324. doi: 10.1105/tpc.18.00872.

Abstract
Small RNAs (sRNAs) that are 21 to 24 nucleotides (nt) in length are found in most eukaryotic organisms and regulate numerous biological functions, including transposon silencing, development, reproduction, and stress responses, typically via control of the stability and/or translation of target mRNAs. Major classes of sRNAs in plants include microRNAs (miRNAs) and small interfering RNAs (siRNAs); sRNAs are known to travel as a silencing signal from cell to cell, root to shoot, and even between host and pathogen. In mammals, sRNAs are transported inside extracellular vesicles (EVs), which are mobile membrane-bound compartments that participate in intercellular communication. In addition to sRNAs, EVs carry proteins, lipids, metabolites, and potentially other types of nucleic acids. Here we report that Arabidopsis (Arabidopsis thaliana) EVs also contain diverse species of sRNA. We found that specific miRNAs and siRNAs are preferentially loaded into plant EVs. We also report a previously overlooked class of “tiny RNAs” (10 to 17 nt) that are highly enriched in EVs. This RNA category of unknown function has a broad and very diverse genome origin and might correspond to degradation products.

100 Most Recent Publications

Bélanger, S, Pokhrel, S, Czymmek, KJ, Meyers, BC. Pre-meiotic, 24-nt reproductive phasiRNAs are abundant in anthers of wheat and barley but not rice and maize. Plant Physiol. 2020; :. doi: 10.1104/pp.20.00816. PubMed PMID:32917771 .

Ding, B, Xia, R, Lin, Q, Gurung, V, Sagawa, JM, Stanley, LE et al.. Developmental Genetics of Corolla Tube Formation: Role of the tasiRNA-ARF Pathway and a Conceptual Model. Plant Cell. 2020; :. doi: 10.1105/tpc.18.00471. PubMed PMID:32917737 .

Eckardt, N, Meyers, BC. Editorial: Sowing the Seeds of Equity and Diversity in Academia and STEM Disciplines. Plant Cell. 2020; :. doi: 10.1105/tpc.20.00692. PubMed PMID:32873630 .

Liu, Y, Teng, C, Xia, R, Meyers, BC. Phased Secondary Small Interfering RNAs (phasiRNAs) in Plants: Their Biogenesis, Genic Sources, and Roles in Stress Responses, Development, and Reproduction. Plant Cell. 2020; :. doi: 10.1105/tpc.20.00335. PubMed PMID:32817252 .

Huang, K, Demirci, F, Batish, M, Treible, W, Meyers, BC, Caplan, JL et al.. Quantitative, super-resolution localization of small RNAs with sRNA-PAINT. Nucleic Acids Res. 2020;48 (16):e96. doi: 10.1093/nar/gkaa623. PubMed PMID:32716042 .

Huang, K, Batish, M, Teng, C, Harkess, A, Meyers, BC, Caplan, JL et al.. Quantitative Fluorescence In Situ Hybridization Detection of Plant mRNAs with Single-Molecule Resolution. Methods Mol. Biol. 2020;2166 :23-33. doi: 10.1007/978-1-0716-0712-1_2. PubMed PMID:32710401 .

Grover, JW, Burgess, D, Kendall, T, Baten, A, Pokhrel, S, King, GJ et al.. Abundant expression of maternal siRNAs is a conserved feature of seed development. Proc. Natl. Acad. Sci. U.S.A. 2020;117 (26):15305-15315. doi: 10.1073/pnas.2001332117. PubMed PMID:32541052 PubMed Central PMC7334491.

Teng, C, Zhang, H, Hammond, R, Huang, K, Meyers, BC, Walbot, V et al.. Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize. Nat Commun. 2020;11 (1):2912. doi: 10.1038/s41467-020-16634-6. PubMed PMID:32518237 PubMed Central PMC7283321.

Jiang, N, Gutierrez-Diaz, A, Mukundi, E, Lee, YS, Meyers, BC, Otegui, MS et al.. Synergy between the anthocyanin and RDR6/SGS3/DCL4 siRNA pathways expose hidden features of Arabidopsis carbon metabolism. Nat Commun. 2020;11 (1):2456. doi: 10.1038/s41467-020-16289-3. PubMed PMID:32415123 PubMed Central PMC7229025.

Harkess, A, Huang, K, van der Hulst, R, Tissen, B, Caplan, JL, Koppula, A et al.. Sex Determination by Two Y-Linked Genes in Garden Asparagus. Plant Cell. 2020;32 (6):1790-1796. doi: 10.1105/tpc.19.00859. PubMed PMID:32220850 PubMed Central PMC7268802.

Hossain, MS, Hoang, NT, Yan, Z, Tóth, K, Meyers, BC, Stacey, G et al.. Corrigendum: Characterization of the Spatial and Temporal Expression of Two Soybean miRNAs Identifies SCL6 as a Novel Regulator of Soybean Nodulation. ;10 :1692. doi: 10.3389/fpls.2019.01692. PubMed PMID:32117326 PubMed Central PMC7029589.

Debladis, E, Lee, TF, Huang, YJ, Lu, JH, Mathioni, SM, Carpentier, MC et al.. Construction and characterization of a knock-down RNA interference line of OsNRPD1 in rice (Oryza sativa ssp japonica cv Nipponbare). Philos. Trans. R. Soc. Lond., B, Biol. Sci. 2020;375 (1795):20190338. doi: 10.1098/rstb.2019.0338. PubMed PMID:32075556 PubMed Central PMC7061988.

Feng, L, Zhang, F, Zhang, H, Zhao, Y, Meyers, BC, Zhai, J et al.. An Online Database for Exploring Over 2,000 Arabidopsis Small RNA Libraries. Plant Physiol. 2020;182 (2):685-691. doi: 10.1104/pp.19.00959. PubMed PMID:31843802 PubMed Central PMC6997705.

Bi, H, Fei, Q, Li, R, Liu, B, Xia, R, Char, SN et al.. Disruption of miRNA sequences by TALENs and CRISPR/Cas9 induces varied lengths of miRNA production. Plant Biotechnol. J. 2020;18 (7):1526-1536. doi: 10.1111/pbi.13315. PubMed PMID:31821678 PubMed Central PMC7292542.

Nakano, M, McCormick, K, Demirci, C, Demirci, F, Gurazada, SGR, Ramachandruni, D et al.. Next-Generation Sequence Databases: RNA and Genomic Informatics Resources for Plants. Plant Physiol. 2020;182 (1):136-146. doi: 10.1104/pp.19.00957. PubMed PMID:31690707 PubMed Central PMC6945852.

Juárez-González, VT, López-Ruiz, BA, Baldrich, P, Luján-Soto, E, Meyers, BC, Dinkova, TD et al.. The explant developmental stage profoundly impacts small RNA-mediated regulation at the dedifferentiation step of maize somatic embryogenesis. Sci Rep. 2019;9 (1):14511. doi: 10.1038/s41598-019-50962-y. PubMed PMID:31601893 PubMed Central PMC6786999.

Crisp, PA, Hammond, R, Zhou, P, Vaillancourt, B, Lipzen, A, Daum, C et al.. Variation and Inheritance of Small RNAs in Maize Inbreds and F1 Hybrids. Plant Physiol. 2020;182 (1):318-331. doi: 10.1104/pp.19.00817. PubMed PMID:31575624 PubMed Central PMC6945832.

Hunt, M, Banerjee, S, Surana, P, Liu, M, Fuerst, G, Mathioni, S et al.. Correction to: small RNA discovery in the interaction between barley and the powdery mildew pathogen. BMC Genomics. 2019;20 (1):697. doi: 10.1186/s12864-019-6012-7. PubMed PMID:31484492 PubMed Central PMC6727339.

Baldrich, P, Meyers, BC. Bacteria send messages to colonize plant roots. Science. 2019;365 (6456):868-869. doi: 10.1126/science.aay7101. PubMed PMID:31467211 .

Ji, L, Mathioni, SM, Johnson, S, Tucker, D, Bewick, AJ, Do Kim, K et al.. Genome-Wide Reinforcement of DNA Methylation Occurs during Somatic Embryogenesis in Soybean. Plant Cell. 2019;31 (10):2315-2331. doi: 10.1105/tpc.19.00255. PubMed PMID:31439802 PubMed Central PMC6790092.

Hunt, M, Banerjee, S, Surana, P, Liu, M, Fuerst, G, Mathioni, S et al.. Small RNA discovery in the interaction between barley and the powdery mildew pathogen. BMC Genomics. 2019;20 (1):610. doi: 10.1186/s12864-019-5947-z. PubMed PMID:31345162 PubMed Central PMC6657096.

Trolet, A, Baldrich, P, Criqui, MC, Dubois, M, Clavel, M, Meyers, BC et al.. Cell Cycle-Dependent Regulation and Function of ARGONAUTE1 in Plants. Plant Cell. 2019;31 (8):1734-1750. doi: 10.1105/tpc.19.00069. PubMed PMID:31189739 PubMed Central PMC6713298.

Hossain, MS, Hoang, NT, Yan, Z, Tóth, K, Meyers, BC, Stacey, G et al.. Characterization of the Spatial and Temporal Expression of Two Soybean miRNAs Identifies SCL6 as a Novel Regulator of Soybean Nodulation. 2019;10 :475. doi: 10.3389/fpls.2019.00475. PubMed PMID:31057581 PubMed Central PMC6477095.

Meyers, BC, Axtell, MJ. MicroRNAs in Plants: Key Findings from the Early Years. Plant Cell. 2019;31 (6):1206-1207. doi: 10.1105/tpc.19.00310. PubMed PMID:31036598 PubMed Central PMC6588298.

Fourounjian, P, Tang, J, Tanyolac, B, Feng, Y, Gelfand, B, Kakrana, A et al.. Post-transcriptional adaptation of the aquatic plant Spirodela polyrhiza under stress and hormonal stimuli. Plant J. 2019;98 (6):1120-1133. doi: 10.1111/tpj.14294. PubMed PMID:30801806 .

Xia, R, Chen, C, Pokhrel, S, Ma, W, Huang, K, Patel, P et al.. 24-nt reproductive phasiRNAs are broadly present in angiosperms. Nat Commun. 2019;10 (1):627. doi: 10.1038/s41467-019-08543-0. PubMed PMID:30733503 PubMed Central PMC6367383.

Baldrich, P, Rutter, BD, Karimi, HZ, Podicheti, R, Meyers, BC, Innes, RW et al.. Plant Extracellular Vesicles Contain Diverse Small RNA Species and Are Enriched in 10- to 17-Nucleotide "Tiny" RNAs. Plant Cell. 2019;31 (2):315-324. doi: 10.1105/tpc.18.00872. PubMed PMID:30705133 PubMed Central PMC6447009.

Huang, K, Baldrich, P, Meyers, BC, Caplan, JL. sRNA-FISH: versatile fluorescent in situ detection of small RNAs in plants. Plant J. 2019;98 (2):359-369. doi: 10.1111/tpj.14210. PubMed PMID:30577085 PubMed Central PMC6465150.

Wittmeyer, K, Cui, J, Chatterjee, D, Lee, TF, Tan, Q, Xue, W et al.. The Dominant and Poorly Penetrant Phenotypes of Maize Unstable factor for orange1 Are Caused by DNA Methylation Changes at a Linked Transposon. Plant Cell. 2018;30 (12):3006-3023. doi: 10.1105/tpc.18.00546. PubMed PMID:30563848 PubMed Central PMC6354275.

Moro, B, Chorostecki, U, Arikit, S, Suarez, IP, Höbartner, C, Rasia, RM et al.. Efficiency and precision of microRNA biogenesis modes in plants. Nucleic Acids Res. 2018;46 (20):10709-10723. doi: 10.1093/nar/gky853. PubMed PMID:30289546 PubMed Central PMC6237749.

Raman, V, Meyers, BC, Dean, RA, Donofrio, NM. Characterizing Small RNAs in Filamentous Fungi Using the Rice Blast Fungus, Magnaporthe oryzae, as an Example. Methods Mol. Biol. 2018;1848 :53-66. doi: 10.1007/978-1-4939-8724-5_5. PubMed PMID:30182228 .

Patel, P, Mathioni, S, Kakrana, A, Shatkay, H, Meyers, BC. Reproductive phasiRNAs in grasses are compositionally distinct from other classes of small RNAs. New Phytol. 2018;220 (3):851-864. doi: 10.1111/nph.15349. PubMed PMID:30020552 .

Fei, Q, Yu, Y, Liu, L, Zhang, Y, Baldrich, P, Dai, Q et al.. Biogenesis of a 22-nt microRNA in Phaseoleae species by precursor-programmed uridylation. Proc. Natl. Acad. Sci. U.S.A. 2018;115 (31):8037-8042. doi: 10.1073/pnas.1807403115. PubMed PMID:30012624 PubMed Central PMC6077734.

Richard, MMS, Gratias, A, Meyers, BC, Geffroy, V. Molecular mechanisms that limit the costs of NLR-mediated resistance in plants. Mol. Plant Pathol. 2018;19 (11):2516-2523. doi: 10.1111/mpp.12723. PubMed PMID:30011120 PubMed Central PMC6638094.

Kakrana, A, Mathioni, SM, Huang, K, Hammond, R, Vandivier, L, Patel, P et al.. Plant 24-nt reproductive phasiRNAs from intramolecular duplex mRNAs in diverse monocots. Genome Res. 2018;28 (9):1333-1344. doi: 10.1101/gr.228163.117. PubMed PMID:30002159 PubMed Central PMC6120631.

Tamim, S, Cai, Z, Mathioni, SM, Zhai, J, Teng, C, Zhang, Q et al.. Cis-directed cleavage and nonstoichiometric abundances of 21-nucleotide reproductive phased small interfering RNAs in grasses. New Phytol. 2018;220 (3):865-877. doi: 10.1111/nph.15181. PubMed PMID:29708601 .

He, J, Xu, M, Willmann, MR, McCormick, K, Hu, T, Yang, L et al.. Threshold-dependent repression of SPL gene expression by miR156/miR157 controls vegetative phase change in Arabidopsis thaliana. PLoS Genet. 2018;14 (4):e1007337. doi: 10.1371/journal.pgen.1007337. PubMed PMID:29672610 PubMed Central PMC5929574.

Edger, PP, Hall, JC, Harkess, A, Tang, M, Coombs, J, Mohammadin, S et al.. Brassicales phylogeny inferred from 72 plastid genes: A reanalysis of the phylogenetic localization of two paleopolyploid events and origin of novel chemical defenses. Am. J. Bot. 2018;105 (3):463-469. doi: 10.1002/ajb2.1040. PubMed PMID:29574686 .

Liu, H, Soyars, CL, Li, J, Fei, Q, He, G, Peterson, BA et al.. CRISPR/Cas9-mediated resistance to cauliflower mosaic virus. 2018;2 (3):e00047. doi: 10.1002/pld3.47. PubMed PMID:31245713 PubMed Central PMC6508564.

van der Linde, K, Timofejeva, L, Egger, RL, Ilau, B, Hammond, R, Teng, C et al.. Pathogen Trojan Horse Delivers Bioactive Host Protein to Alter Maize Anther Cell Behavior in Situ. Plant Cell. 2018;30 (3):528-542. doi: 10.1105/tpc.17.00238. PubMed PMID:29449414 PubMed Central PMC5894838.

Baldrich, P, Beric, A, Meyers, BC. Despacito: the slow evolutionary changes in plant microRNAs. Curr. Opin. Plant Biol. 2018;42 :16-22. doi: 10.1016/j.pbi.2018.01.007. PubMed PMID:29448158 .

Axtell, MJ, Meyers, BC. Revisiting Criteria for Plant MicroRNA Annotation in the Era of Big Data. Plant Cell. 2018;30 (2):272-284. doi: 10.1105/tpc.17.00851. PubMed PMID:29343505 PubMed Central PMC5868703.

Ma, W, Chen, C, Liu, Y, Zeng, M, Meyers, BC, Li, J et al.. Coupling of microRNA-directed phased small interfering RNA generation from long noncoding genes with alternative splicing and alternative polyadenylation in small RNA-mediated gene silencing. New Phytol. 2018;217 (4):1535-1550. doi: 10.1111/nph.14934. PubMed PMID:29218722 .

Friesner, J, Assmann, SM, Bastow, R, Bailey-Serres, J, Beynon, J, Brendel, V et al.. The Next Generation of Training for Arabidopsis Researchers: Bioinformatics and Quantitative Biology. Plant Physiol. 2017;175 (4):1499-1509. doi: 10.1104/pp.17.01490. PubMed PMID:29208732 PubMed Central PMC5717721.

Wang, PH, Wittmeyer, KT, Lee, TF, Meyers, BC, Chopra, S. Overlapping RdDM and non-RdDM mechanisms work together to maintain somatic repression of a paramutagenic epiallele of maize pericarp color1. PLoS ONE. 2017;12 (11):e0187157. doi: 10.1371/journal.pone.0187157. PubMed PMID:29112965 PubMed Central PMC5675401.

Harkess, A, Zhou, J, Xu, C, Bowers, JE, Van der Hulst, R, Ayyampalayam, S et al.. The asparagus genome sheds light on the origin and evolution of a young Y chromosome. Nat Commun. 2017;8 (1):1279. doi: 10.1038/s41467-017-01064-8. PubMed PMID:29093472 PubMed Central PMC5665984.

Sidorenko, LV, Lee, TF, Woosley, A, Moskal, WA, Bevan, SA, Merlo, PAO et al.. GC-rich coding sequences reduce transposon-like, small RNA-mediated transgene silencing. Nat Plants. 2017;3 (11):875-884. doi: 10.1038/s41477-017-0040-6. PubMed PMID:29085072 .

Wai, CM, VanBuren, R, Zhang, J, Huang, L, Miao, W, Edger, PP et al.. Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple. Plant J. 2017;92 (1):19-30. doi: 10.1111/tpj.13630. PubMed PMID:28670834 .

Huang, K, Doyle, F, Wurz, ZE, Tenenbaum, SA, Hammond, RK, Caplan, JL et al.. FASTmiR: an RNA-based sensor for in vitro quantification and live-cell localization of small RNAs. Nucleic Acids Res. 2017;45 (14):e130. doi: 10.1093/nar/gkx504. PubMed PMID:28586459 PubMed Central PMC5737440.

Raman, V, Simon, SA, Demirci, F, Nakano, M, Meyers, BC, Donofrio, NM et al.. Small RNA Functions Are Required for Growth and Development of Magnaporthe oryzae. Mol. Plant Microbe Interact. 2017;30 (7):517-530. doi: 10.1094/MPMI-11-16-0236-R. PubMed PMID:28504560 .

Xia, R, Xu, J, Meyers, BC. The Emergence, Evolution, and Diversification of the miR390-TAS3-ARF Pathway in Land Plants. Plant Cell. 2017;29 (6):1232-1247. doi: 10.1105/tpc.17.00185. PubMed PMID:28442597 PubMed Central PMC5502456.

Reyes-Chin-Wo, S, Wang, Z, Yang, X, Kozik, A, Arikit, S, Song, C et al.. Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce. Nat Commun. 2017;8 :14953. doi: 10.1038/ncomms14953. PubMed PMID:28401891 PubMed Central PMC5394340.

Mathioni, SM, Kakrana, A, Meyers, BC. Characterization of Plant Small RNAs by Next Generation Sequencing. Curr Protoc Plant Biol. 2017;2 (1):39-63. doi: 10.1002/cppb.20043. PubMed PMID:31725976 .

Yu, Y, Ji, L, Le, BH, Zhai, J, Chen, J, Luscher, E et al.. ARGONAUTE10 promotes the degradation of miR165/6 through the SDN1 and SDN2 exonucleases in Arabidopsis. PLoS Biol. 2017;15 (2):e2001272. doi: 10.1371/journal.pbio.2001272. PubMed PMID:28231321 PubMed Central PMC5322904.

Fan, Y, Yang, J, Mathioni, SM, Yu, J, Shen, J, Yang, X et al.. PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc. Natl. Acad. Sci. U.S.A. 2016;113 (52):15144-15149. doi: 10.1073/pnas.1619159114. PubMed PMID:27965387 PubMed Central PMC5206514.

Nan, GL, Zhai, J, Arikit, S, Morrow, D, Fernandes, J, Mai, L et al.. MS23, a master basic helix-loop-helix factor, regulates the specification and development of the tapetum in maize. Development. 2017;144 (1):163-172. doi: 10.1242/dev.140673. PubMed PMID:27913638 .

Fei, Q, Yang, L, Liang, W, Zhang, D, Meyers, BC. Dynamic changes of small RNAs in rice spikelet development reveal specialized reproductive phasiRNA pathways. J. Exp. Bot. 2016;67 (21):6037-6049. doi: 10.1093/jxb/erw361. PubMed PMID:27702997 PubMed Central PMC5100018.

Paim Pinto, DL, Brancadoro, L, Dal Santo, S, De Lorenzis, G, Pezzotti, M, Meyers, BC et al.. The Influence of Genotype and Environment on Small RNA Profiles in Grapevine Berry. 2016;7 :1459. doi: 10.3389/fpls.2016.01459. PubMed PMID:27761135 PubMed Central PMC5050227.

Zhang, Y, Xia, R, Kuang, H, Meyers, BC. The Diversification of Plant NBS-LRR Defense Genes Directs the Evolution of MicroRNAs That Target Them. Mol. Biol. Evol. 2016;33 (10):2692-705. doi: 10.1093/molbev/msw154. PubMed PMID:27512116 PubMed Central PMC5026261.

Char, SN, Neelakandan, AK, Nahampun, H, Frame, B, Main, M, Spalding, MH et al.. An Agrobacterium-delivered CRISPR/Cas9 system for high-frequency targeted mutagenesis in maize. Plant Biotechnol. J. 2017;15 (2):257-268. doi: 10.1111/pbi.12611. PubMed PMID:27510362 PubMed Central PMC5259581.

Yang, L, Qian, X, Chen, M, Fei, Q, Meyers, BC, Liang, W et al.. Regulatory Role of a Receptor-Like Kinase in Specifying Anther Cell Identity. Plant Physiol. 2016;171 (3):2085-100. doi: 10.1104/pp.16.00016. PubMed PMID:27208278 PubMed Central PMC4936546.

Wendel, JF, Jackson, SA, Meyers, BC, Wing, RA. Evolution of plant genome architecture. Genome Biol. 2016;17 :37. doi: 10.1186/s13059-016-0908-1. PubMed PMID:26926526 PubMed Central PMC4772531.

Fei, Q, Zhang, Y, Xia, R, Meyers, BC. Small RNAs Add Zing to the Zig-Zag-Zig Model of Plant Defenses. Mol. Plant Microbe Interact. 2016;29 (3):165-9. doi: 10.1094/MPMI-09-15-0212-FI. PubMed PMID:26867095 .

Khatabi, B, Arikit, S, Xia, R, Winter, S, Oumar, D, Mongomake, K et al.. High-resolution identification and abundance profiling of cassava (Manihot esculenta Crantz) microRNAs. BMC Genomics. 2016;17 :85. doi: 10.1186/s12864-016-2391-1. PubMed PMID:26822616 PubMed Central PMC4730657.

Curtin, SJ, Michno, JM, Campbell, BW, Gil-Humanes, J, Mathioni, SM, Hammond, R et al.. MicroRNA Maturation and MicroRNA Target Gene Expression Regulation Are Severely Disrupted in Soybean dicer-like1 Double Mutants. G3 (Bethesda). 2015;6 (2):423-33. doi: 10.1534/g3.115.022137. PubMed PMID:26681515 PubMed Central PMC4751560.

Patel, P, Ramachandruni, SD, Kakrana, A, Nakano, M, Meyers, BC. miTRATA: a web-based tool for microRNA Truncation and Tailing Analysis. Bioinformatics. 2016;32 (3):450-2. doi: 10.1093/bioinformatics/btv583. PubMed PMID:26454275 .

Zhai, J, Bischof, S, Wang, H, Feng, S, Lee, TF, Teng, C et al.. A One Precursor One siRNA Model for Pol IV-Dependent siRNA Biogenesis. Cell. 2015;163 (2):445-55. doi: 10.1016/j.cell.2015.09.032. PubMed PMID:26451488 PubMed Central PMC5023148.

Cao, X, Meyers, BC. Editorial overview: Cell signalling and gene regulation-communication and control as the twin pillars of systems biology. Curr. Opin. Plant Biol. 2015;27 :v-viii. doi: 10.1016/j.pbi.2015.09.001. PubMed PMID:26433830 .

Xia, R, Xu, J, Arikit, S, Meyers, BC. Extensive Families of miRNAs and PHAS Loci in Norway Spruce Demonstrate the Origins of Complex phasiRNA Networks in Seed Plants. Mol. Biol. Evol. 2015;32 (11):2905-18. doi: 10.1093/molbev/msv164. PubMed PMID:26318183 PubMed Central PMC4651229.

Zhang, H, Xia, R, Meyers, BC, Walbot, V. Evolution, functions, and mysteries of plant ARGONAUTE proteins. Curr. Opin. Plant Biol. 2015;27 :84-90. doi: 10.1016/j.pbi.2015.06.011. PubMed PMID:26190741 .

Xia, R, Ye, S, Liu, Z, Meyers, BC, Liu, Z. Novel and Recently Evolved MicroRNA Clusters Regulate Expansive F-BOX Gene Networks through Phased Small Interfering RNAs in Wild Diploid Strawberry. Plant Physiol. 2015;169 (1):594-610. doi: 10.1104/pp.15.00253. PubMed PMID:26143249 PubMed Central PMC4577376.

Fei, Q, Li, P, Teng, C, Meyers, BC. Secondary siRNAs from Medicago NB-LRRs modulated via miRNA-target interactions and their abundances. Plant J. 2015;83 (3):451-65. doi: 10.1111/tpj.12900. PubMed PMID:26042408 .

Belli Kullan, J, Lopes Paim Pinto, D, Bertolini, E, Fasoli, M, Zenoni, S, Tornielli, GB et al.. miRVine: a microRNA expression atlas of grapevine based on small RNA sequencing. BMC Genomics. 2015;16 :393. doi: 10.1186/s12864-015-1610-5. PubMed PMID:25981679 PubMed Central PMC4434875.

Yan, Z, Hossain, MS, Valdés-López, O, Hoang, NT, Zhai, J, Wang, J et al.. Identification and functional characterization of soybean root hair microRNAs expressed in response to Bradyrhizobium japonicum infection. Plant Biotechnol. J. 2016;14 (1):332-41. doi: 10.1111/pbi.12387. PubMed PMID:25973713 .

Tu, B, Liu, L, Xu, C, Zhai, J, Li, S, Lopez, MA et al.. Distinct and cooperative activities of HESO1 and URT1 nucleotidyl transferases in microRNA turnover in Arabidopsis. PLoS Genet. 2015;11 (4):e1005119. doi: 10.1371/journal.pgen.1005119. PubMed PMID:25928405 PubMed Central PMC4415760.

El Baidouri, M, Kim, KD, Abernathy, B, Arikit, S, Maumus, F, Panaud, O et al.. A new approach for annotation of transposable elements using small RNA mapping. Nucleic Acids Res. 2015;43 (13):e84. doi: 10.1093/nar/gkv257. PubMed PMID:25813049 PubMed Central PMC4513842.

Yan, Z, Hossain, MS, Arikit, S, Valdés-López, O, Zhai, J, Wang, J et al.. Identification of microRNAs and their mRNA targets during soybean nodule development: functional analysis of the role of miR393j-3p in soybean nodulation. New Phytol. 2015;207 (3):748-59. doi: 10.1111/nph.13365. PubMed PMID:25783944 .

Zhao, M, Meyers, BC, Cai, C, Xu, W, Ma, J. Evolutionary patterns and coevolutionary consequences of MIRNA genes and microRNA targets triggered by multiple mechanisms of genomic duplications in soybean. Plant Cell. 2015;27 (3):546-62. doi: 10.1105/tpc.15.00048. PubMed PMID:25747880 PubMed Central PMC4558674.

Zhai, J, Zhang, H, Arikit, S, Huang, K, Nan, GL, Walbot, V et al.. Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. Proc. Natl. Acad. Sci. U.S.A. 2015;112 (10):3146-51. doi: 10.1073/pnas.1418918112. PubMed PMID:25713378 PubMed Central PMC4364226.

Arikit, S, Xia, R, Kakrana, A, Huang, K, Zhai, J, Yan, Z et al.. An atlas of soybean small RNAs identifies phased siRNAs from hundreds of coding genes. Plant Cell. 2014;26 (12):4584-601. doi: 10.1105/tpc.114.131847. PubMed PMID:25465409 PubMed Central PMC4311202.

Thompson, BE, Basham, C, Hammond, R, Ding, Q, Kakrana, A, Lee, TF et al.. The dicer-like1 homolog fuzzy tassel is required for the regulation of meristem determinacy in the inflorescence and vegetative growth in maize. Plant Cell. 2014;26 (12):4702-17. doi: 10.1105/tpc.114.132670. PubMed PMID:25465405 PubMed Central PMC4311206.

Kakrana, A, Hammond, R, Patel, P, Nakano, M, Meyers, BC. sPARTA: a parallelized pipeline for integrated analysis of plant miRNA and cleaved mRNA data sets, including new miRNA target-identification software. Nucleic Acids Res. 2014;42 (18):e139. doi: 10.1093/nar/gku693. PubMed PMID:25120269 PubMed Central PMC4191380.

Cantó-Pastor, A, Mollá-Morales, A, Ernst, E, Dahl, W, Zhai, J, Yan, Y et al.. Efficient transformation and artificial miRNA gene silencing in Lemna minor. Plant Biol (Stuttg). 2015;17 Suppl 1 :59-65. doi: 10.1111/plb.12215. PubMed PMID:24989135 PubMed Central PMC4458260.

Wong, J, Gao, L, Yang, Y, Zhai, J, Arikit, S, Yu, Y et al.. Roles of small RNAs in soybean defense against Phytophthora sojae infection. Plant J. 2014;79 (6):928-40. doi: 10.1111/tpj.12590. PubMed PMID:24944042 PubMed Central PMC5137376.

Sasaki, T, Lee, TF, Liao, WW, Naumann, U, Liao, JL, Eun, C et al.. Distinct and concurrent pathways of Pol II- and Pol IV-dependent siRNA biogenesis at a repetitive trans-silencer locus in Arabidopsis thaliana. Plant J. 2014;79 (1):127-38. doi: 10.1111/tpj.12545. PubMed PMID:24798377 .

Gregory, BD, Meyers, BC. Genomic approaches for studying transcriptional and post-transcriptional processes. Methods. 2014;67 (1):1-2. doi: 10.1016/j.ymeth.2014.03.025. PubMed PMID:24766879 .

Chávez Montes, RA, de Fátima Rosas-Cárdenas, F, De Paoli, E, Accerbi, M, Rymarquis, LA, Mahalingam, G et al.. Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nat Commun. 2014;5 :3722. doi: 10.1038/ncomms4722. PubMed PMID:24759728 .

Venu, RC, Ma, J, Jia, Y, Liu, G, Jia, MH, Nobuta, K et al.. Identification of candidate genes associated with positive and negative heterosis in rice. PLoS ONE. 2014;9 (4):e95178. doi: 10.1371/journal.pone.0095178. PubMed PMID:24743656 PubMed Central PMC3990613.

Schapire, AL, Bologna, NG, Moro, B, Zhai, J, Meyers, BC, Palatnik, JF et al.. Reprint of: construction of Specific Parallel Amplification of RNA Ends (SPARE) libraries for the systematic identification of plant microRNA processing intermediates. Methods. 2014;67 (1):36-44. doi: 10.1016/j.ymeth.2014.04.001. PubMed PMID:24731939 .

Creasey, KM, Zhai, J, Borges, F, Van Ex, F, Regulski, M, Meyers, BC et al.. miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature. 2014;508 (7496):411-5. doi: 10.1038/nature13069. PubMed PMID:24670663 PubMed Central PMC4074602.

Wei, L, Gu, L, Song, X, Cui, X, Lu, Z, Zhou, M et al.. Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc. Natl. Acad. Sci. U.S.A. 2014;111 (10):3877-82. doi: 10.1073/pnas.1318131111. PubMed PMID:24554078 PubMed Central PMC3956178.

Jeong, DH, Schmidt, SA, Rymarquis, LA, Park, S, Ganssmann, M, German, MA et al.. Parallel analysis of RNA ends enhances global investigation of microRNAs and target RNAs of Brachypodium distachyon. Genome Biol. 2013;14 (12):R145. doi: 10.1186/gb-2013-14-12-r145. PubMed PMID:24367943 PubMed Central PMC4053937.

Amborella Genome Project. The Amborella genome and the evolution of flowering plants. Science. 2013;342 (6165):1241089. doi: 10.1126/science.1241089. PubMed PMID:24357323 .

Venkataramanan, KP, Jones, SW, McCormick, KP, Kunjeti, SG, Ralston, MT, Meyers, BC et al.. The Clostridium small RNome that responds to stress: the paradigm and importance of toxic metabolite stress in C. acetobutylicum. BMC Genomics. 2013;14 :849. doi: 10.1186/1471-2164-14-849. PubMed PMID:24299206 PubMed Central PMC3879012.

Gong, L, Kakrana, A, Arikit, S, Meyers, BC, Wendel, JF. Composition and expression of conserved microRNA genes in diploid cotton (Gossypium) species. Genome Biol Evol. 2013;5 (12):2449-59. doi: 10.1093/gbe/evt196. PubMed PMID:24281048 PubMed Central PMC3879982.

Schapire, AL, Bologna, NG, Moro, B, Zhai, J, Meyers, BC, Palatnik, JF et al.. Construction of Specific Parallel Amplification of RNA Ends (SPARE) libraries for the systematic identification of plant microRNA processing intermediates. Methods. 2013;64 (3):283-91. doi: 10.1016/j.ymeth.2013.08.032. PubMed PMID:24018204 .

McDowell, JM, Meyers, BC. A transposable element is domesticated for service in the plant immune system. Proc. Natl. Acad. Sci. U.S.A. 2013;110 (37):14821-2. doi: 10.1073/pnas.1314089110. PubMed PMID:23995444 PubMed Central PMC3773748.

Bologna, NG, Schapire, AL, Zhai, J, Chorostecki, U, Boisbouvier, J, Meyers, BC et al.. Multiple RNA recognition patterns during microRNA biogenesis in plants. Genome Res. 2013;23 (10):1675-89. doi: 10.1101/gr.153387.112. PubMed PMID:23990609 PubMed Central PMC3787264.

Fei, Q, Xia, R, Meyers, BC. Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell. 2013;25 (7):2400-15. doi: 10.1105/tpc.113.114652. PubMed PMID:23881411 PubMed Central PMC3753373.

Zhai, J, Zhao, Y, Simon, SA, Huang, S, Petsch, K, Arikit, S et al.. Plant microRNAs display differential 3' truncation and tailing modifications that are ARGONAUTE1 dependent and conserved across species. Plant Cell. 2013;25 (7):2417-28. doi: 10.1105/tpc.113.114603. PubMed PMID:23839787 PubMed Central PMC3753374.

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