Multiomics studies with co-transformation reveal microRNAs via miRNA-TF-mRNA network participating in wood formation in Hevea brasiliensis

Introduction MicroRNAs (miRNAs) are small endogenous non-coding RNAs that play an important role in wood formation in plants. However, the significance of the link between miRNAs and their target transcripts in wood formation remains unclear in rubber tree (Hevea brasiliensis). Methods In this study, we induced the formation of reaction wood by artificially bending rubber trees for 300 days and performed small RNA sequencing and transcriptome deep sequencing (RNA-seq) to describe the complement of miRNAs and their targets contributing to this process. Results and discussion We identified 5, 11, and 2 differentially abundant miRNAs in normal wood (NW) compared to tension wood (TW), in NW relative to opposite wood (OW), and between TW and OW, respectively. We also identified 12 novel miRNAs and 39 potential miRNA-mRNA pairs with different accumulation patterns in NW, TW, and OW. We noticed that many miRNAs targeted transcription factor genes, which were enriched in KEGG pathways associated with phenylpropanoid biosynthesis, phenylalanine metabolism, and pyruvate metabolism. Thus, miRNA-TF-mRNA network involved in wood formation via tension wood model were constructed. We validated the differential accumulation of miRNAs and their targets by RT-qPCR analysis and overexpressed miRNA in Nicotiana benthamiana with its potential target gene. These results will provide a reference for a deep exploration of growth and development in rubber tree.

[1]  Q. Du,et al.  Pyramiding superior haplotypes and epistatic alleles to accelerate wood quality and yield improvement in poplar breeding , 2021 .

[2]  Jia Li,et al.  RNA Sequencing Reveals Phenylpropanoid Biosynthesis Genes and Transcription Factors for Hevea brasiliensis Reaction Wood Formation , 2021, Frontiers in Genetics.

[3]  Thanunchanok Chairin,et al.  Roles of systemic fungicide in antifungal activity and induced defense responses in rubber tree (Hevea brasiliensis) against leaf fall disease caused by Neopestalotiopsis cubana , 2020 .

[4]  Shuang Wu,et al.  MiR319a-Targeted PtoTCP20 Regulates Secondary Growth via interactions with PtoWOX4 and PtoWND6 in Populus tomentosa. , 2020, The New phytologist.

[5]  Yan Lu,et al.  MicroRNA comparison between poplar and larch provides insight into the different mechanism of wood formation , 2020, Plant Cell Reports.

[6]  Xinyi Yu,et al.  MicroRNA397b negatively regulates resistance of Malus hupehensis to Botryosphaeria dothidea by modulating MhLAC7 involved in lignin biosynthesis. , 2020, Plant science : an international journal of experimental plant biology.

[7]  E. Eichler,et al.  The Chromosome-based Rubber Tree Genome Provides New Insights into Spurge Genome Evolution and Rubber Biosynthesis. , 2019, Molecular plant.

[8]  Weidong Zhu,et al.  Mechanisms and Functions of Long Non-Coding RNAs at Multiple Regulatory Levels , 2019, International journal of molecular sciences.

[9]  W. Boerjan,et al.  Lignin Engineering in Forest Trees , 2019, Front. Plant Sci..

[10]  Chaofeng Li,et al.  Ectopic Expression of PtoMYB74 in Poplar and Arabidopsis Promotes Secondary Cell Wall Formation , 2018, Front. Plant Sci..

[11]  Longxin Wang,et al.  Genetic architecture underlying the lignin biosynthesis pathway involves noncoding RNAs and transcription factors for growth and wood properties in Populus , 2018, Plant biotechnology journal.

[12]  Q. Du,et al.  Association Genetics in Populus Reveal the Allelic Interactions of Pto-MIR167a and Its Targets in Wood Formation , 2018, Front. Plant Sci..

[13]  Alex Bateman,et al.  Non‐Coding RNA Analysis Using the Rfam Database , 2018, Current protocols in bioinformatics.

[14]  X. Dai,et al.  psRNATarget: a plant small RNA target analysis server (2017 release) , 2018, Nucleic Acids Res..

[15]  Arnannit Kuyyogsuy,et al.  Chitosan enhances resistance in rubber tree (Hevea brasiliensis), through the induction of abscisic acid (ABA) , 2018 .

[16]  A. Bacic,et al.  Transcriptome analysis provides insights into xylogenesis formation in Moso bamboo (Phyllostachys edulis) shoot , 2018, Scientific Reports.

[17]  X. Ren,et al.  Genome-wide identification, evolution and expression analysis of cyclic nucleotide-gated channels in tobacco (Nicotiana tabacum L.). , 2018, Genomics.

[18]  Ping Liu,et al.  Identification and comparative profiling of ovarian and testicular microRNAs in the swimming crab Portunus trituberculatus. , 2018, Gene.

[19]  P. Priyadarshan Refinements to Hevea rubber breeding , 2017, Tree Genetics & Genomes.

[20]  Elliot M. Meyerowitz,et al.  Regulation of Meristem Morphogenesis by Cell Wall Synthases in Arabidopsis , 2016, Current Biology.

[21]  Di Fan,et al.  PtoMYB92 is a Transcriptional Activator of the Lignin Biosynthetic Pathway During Secondary Cell Wall Formation in Populus tomentosa. , 2015, Plant & cell physiology.

[22]  Masato Yoshida,et al.  Continuum contraction of tension wood fiber induced by repetitive hygrothermal treatment , 2015, Wood Science and Technology.

[23]  Huanzhong Wang,et al.  The role of HD-ZIP III transcription factors and miR165/166 in vascular development and secondary cell wall formation , 2015, Plant signaling & behavior.

[24]  J. Rencoret,et al.  Cell wall modifications triggered by the down-regulation of Coumarate 3-hydroxylase-1 in maize. , 2015, Plant science : an international journal of experimental plant biology.

[25]  I. Granlund,et al.  The cell biology of lignification in higher plants. , 2015, Annals of botany.

[26]  Xiaohui Yang,et al.  Transcriptome profiling of radiata pine branches reveals new insights into reaction wood formation with implications in plant gravitropism , 2013, BMC Genomics.

[27]  Chaofeng Li,et al.  Functional Characterization of the Poplar R2R3-MYB Transcription Factor PtoMYB216 Involved in the Regulation of Lignin Biosynthesis during Wood Formation , 2013, PloS one.

[28]  R. Sederoff,et al.  Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa , 2013, Proceedings of the National Academy of Sciences.

[29]  H. Ling,et al.  Disruption of secondary wall cellulose biosynthesis alters cadmium translocation and tolerance in rice plants. , 2013, Molecular plant.

[30]  Joaquín Herrero,et al.  Bioinformatic and functional characterization of the basic peroxidase 72 from Arabidopsis thaliana involved in lignin biosynthesis , 2013, Planta.

[31]  Ming Wen,et al.  miREvo: an integrative microRNA evolutionary analysis platform for next-generation sequencing experiments , 2012, BMC Bioinformatics.

[32]  Seema Singh,et al.  Biosynthesis and incorporation of side-chain-truncated lignin monomers to reduce lignin polymerization and enhance saccharification. , 2012, Plant biotechnology journal.

[33]  Sebastian D. Mackowiak,et al.  miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades , 2011, Nucleic acids research.

[34]  Jing Chen,et al.  Integrated Profiling of MicroRNAs and mRNAs: MicroRNAs Located on Xq27.3 Associate with Clear Cell Renal Cell Carcinoma , 2010, PloS one.

[35]  Jørgen Holst Christensen,et al.  Engineering traditional monolignols out of lignin by concomitant up-regulation of F5H1 and down-regulation of COMT in Arabidopsis. , 2010, The Plant journal : for cell and molecular biology.

[36]  H. Mo,et al.  Over-expression of F5H in COMT-deficient Arabidopsis leads to enrichment of an unusual lignin and disruption of pollen wall formation. , 2010, The Plant Journal.

[37]  Robert W. Sykes,et al.  Antisense Down-Regulation of 4CL Expression Alters Lignification, Tree Growth, and Saccharification Potential of Field-Grown Poplar1[W][OA] , 2010, Plant Physiology.

[38]  R. Zhong,et al.  Functional Characterization of Poplar Wood-Associated NAC Domain Transcription Factors1[C][OA] , 2009, Plant Physiology.

[39]  Weixiong Zhang,et al.  Conservation and divergence of microRNAs and their functions in Euphorbiaceous plants , 2009, Nucleic acids research.

[40]  R. Zhong,et al.  Transcriptional regulation of lignin biosynthesis , 2009, Plant signaling & behavior.

[41]  Qian Qian,et al.  A missense mutation in the transmembrane domain of CESA4 affects protein abundance in the plasma membrane and results in abnormal cell wall biosynthesis in rice , 2009, Plant Molecular Biology.

[42]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[43]  J. Ralph,et al.  Suppression of 4-Coumarate-CoA Ligase in the Coniferous Gymnosperm Pinus radiata1[W] , 2008, Plant Physiology.

[44]  Thomas D. Schmittgen,et al.  Analyzing real-time PCR data by the comparative CT method , 2008, Nature Protocols.

[45]  Y. Barrière,et al.  Both caffeoyl Coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignin, flavonoids and sinapoyl malate biosynthesis in Arabidopsis , 2007, Planta.

[46]  Hiroo Fukuda,et al.  Transcriptional regulation in wood formation. , 2007, Trends in plant science.

[47]  Tao Cai,et al.  Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary , 2005, Bioinform..

[48]  Armand Séguin,et al.  CINNAMYL ALCOHOL DEHYDROGENASE-C and -D Are the Primary Genes Involved in Lignin Biosynthesis in the Floral Stem of Arabidopsisw⃞ , 2005, The Plant Cell Online.

[49]  D. Bartel MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[50]  S. Turner,et al.  Interactions among three distinct CesA proteins essential for cellulose synthesis , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[51]  B. Reinhart,et al.  Prediction of Plant MicroRNA Targets , 2002, Cell.

[52]  S. Turner,et al.  Multiple Cellulose Synthase Catalytic Subunits Are Required for Cellulose Synthesis in Arabidopsis , 2000, Plant Cell.

[53]  S. Cutler,et al.  The irregular xylem3 Locus of Arabidopsis Encodes a Cellulose Synthase Required for Secondary Cell Wall Synthesis , 1999, Plant Cell.

[54]  D. Baulcombe,et al.  Requirement of sense transcription for homology‐dependent virus resistance and trans‐inactivation , 1997 .

[55]  C. N. Stewart,et al.  Functional characterization of the switchgrass (Panicum virgatum) R2R3-MYB transcription factor PvMYB4 for improvement of lignocellulosic feedstocks. , 2012, The New phytologist.

[56]  Sébastien Tempel Using and understanding RepeatMasker. , 2012, Methods in molecular biology.

[57]  T. Gorshkova,et al.  Tensional stress generation in gelatinous fibres: a review and possible mechanism based on cell-wall structure and composition. , 2012, Journal of experimental botany.

[58]  K. P. Prabhakaran Nair,et al.  Rubber ( Hevea brasiliensis ) , 2010 .

[59]  J. Cairney,et al.  A simple and efficient method for isolating RNA from pine trees , 1993, Plant Molecular Biology Reporter.