Rice miR1432 Fine-Tunes the Balance of Yield and Blast Disease Resistance via Different Modules

microRNAs act as fine-tuners in the regulation of plant growth and resistance against biotic and abiotic stress. Here we demonstrate that rice miR1432 fine-tunes yield and blast disease resistance via different modules. The expression of miR1432 is differentially regulated in the susceptible and resistance accessions by the infection of the blast fungus Magnaporthe oryzae. Overexpression of miR1432 leads to compromised resistance and decreased yield, whereas blocking miR1432 using a target mimic of miR1432 results in enhanced resistance and yield. Moreover, miR1432 suppresses the expression of LOC_Os03g59790, which encodes an EF-hand family protein 1 (OsEFH1). Overexpression of OsEFH1 leads to enhanced rice resistance but decreased grain yield. Consistently, blocking miR1432 or overexpression of OsEFH1 improves pathogen/microbe-associated molecular pattern- triggered immunity. In contrast, overexpression of ACOT, a previously identified target gene of miR1432 involved in the regulation of rice yield traits, has no significant effects on rice blast disease resistance. Altogether, these results indicate that miR1432 balances yield and resistance via different target genes, and blocking miR1432 can simultaneously improve yield and resistance.

[1]  Tyr Wiesner-Hanks,et al.  Navigating complexity to breed disease-resistant crops , 2017, Nature Reviews Genetics.

[2]  Meng Yuan,et al.  uORF-mediated translation allows engineered plant disease resistance without fitness costs , 2017, Nature.

[3]  S. He,et al.  Pattern-recognition receptors are required for NLR-mediated plant immunity , 2020, Nature.

[4]  Hailing Jin,et al.  Role of small RNAs in host-microbe interactions. , 2010, Annual review of phytopathology.

[5]  J. Ellis,et al.  Acyl Coenzyme A Thioesterase 7 Regulates Neuronal Fatty Acid Metabolism To Prevent Neurotoxicity , 2013, Molecular and Cellular Biology.

[6]  B. San Segundo,et al.  OsDCL1a activation impairs phytoalexin biosynthesis and compromises disease resistance in rice , 2018, Annals of botany.

[7]  Jian-Min Zhou,et al.  Phytopathogen effectors subverting host immunity: different foes, similar battleground. , 2012, Cell host & microbe.

[8]  H. Xue,et al.  miR1432‐OsACOT (Acyl‐CoA thioesterase) module determines grain yield via enhancing grain filling rate in rice , 2018, Plant biotechnology journal.

[9]  F. Liu,et al.  OsRab5a regulates endomembrane organization and storage protein trafficking in rice endosperm cells. , 2010, The Plant journal : for cell and molecular biology.

[10]  H. Vogel,et al.  Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. , 2007, The Biochemical journal.

[11]  Lei Gao,et al.  Genome-Wide Identification and Characterization of microRNAs in Developing Grains of Zea mays L. , 2016, PloS one.

[12]  J. Parker,et al.  Effector-triggered immunity: from pathogen perception to robust defense. , 2015, Annual review of plant biology.

[13]  Jing Fan,et al.  Multiple Rice MicroRNAs Are Involved in Immunity against the Blast Fungus Magnaporthe oryzae1[C][W][OPEN] , 2013, Plant Physiology.

[14]  Ertao Wang,et al.  Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance , 2017, Science.

[15]  M. Todesco,et al.  Target mimicry provides a new mechanism for regulation of microRNA activity , 2007, Nature Genetics.

[16]  Chengcai Chu,et al.  MicroRNAs in crop improvement: fine-tuners for complex traits , 2017, Nature Plants.

[17]  Hongwei Zhao,et al.  Magnaporthe oryzae Induces the Expression of a MicroRNA to Suppress the Immune Response in Rice1[OPEN] , 2018, Plant Physiology.

[18]  Jonathan D. G. Jones,et al.  Mutual potentiation of plant immunity by cell-surface and intracellular receptors , 2020, Nature.

[19]  Publisher's Note , 2018, Anaesthesia.

[20]  Joy Bergelson,et al.  Surveying Patterns in the Cost of Resistance in Plants , 1996, The American Naturalist.

[21]  T. Boller,et al.  Innate Immunity in Plants: An Arms Race Between Pattern Recognition Receptors in Plants and Effectors in Microbial Pathogens , 2009, Science.

[22]  S. Kapoor,et al.  Expression analysis of calcium-dependent protein kinase gene family during reproductive development and abiotic stress conditions in rice (Oryza sativa L. ssp. indica) , 2007, Molecular Genetics and Genomics.

[23]  Shen Chen,et al.  Functional divergence of duplicated genes results in a novel blast resistance gene Pi50 at the Pi2/9 locus , 2015, Theoretical and Applied Genetics.

[24]  N. Hayashi,et al.  Development of monogenic lines of rice for blast resistance , 2000 .

[25]  A. Dodd,et al.  The language of calcium signaling. , 2010, Annual review of plant biology.

[26]  F. Liu,et al.  OsVPS9A functions cooperatively with OsRAB5A to regulate post-Golgi dense vesicle-mediated storage protein trafficking to the protein storage vacuole in rice endosperm cells. , 2013, Molecular plant.

[27]  Jing Fan,et al.  Fine-Tuning Roles of Osa-miR159a in Rice Immunity Against Magnaporthe oryzae and Development , 2021, Rice.

[28]  B. San Segundo,et al.  The Polycistronic miR166k-166h Positively Regulates Rice Immunity via Post-transcriptional Control of EIN2 , 2018, Front. Plant Sci..

[29]  Osa-miR162a fine-tunes rice resistance to Magnaporthe oryzae and Yield , 2020, Rice.

[30]  Elucidating the regulatory roles of microRNAs in maize (Zea mays L.) leaf growth response to chilling stress , 2020, Planta.

[31]  Jing Fan,et al.  Osa-miR167d facilitates infection of Magnaporthe oryzae in rice. , 2020, Journal of integrative plant biology.

[32]  Jun Liu,et al.  Lysin Motif–Containing Proteins LYP4 and LYP6 Play Dual Roles in Peptidoglycan and Chitin Perception in Rice Innate Immunity[W][OA] , 2012, Plant Cell.

[33]  Shanshan Zhu,et al.  A cyclic nucleotide-gated channel mediates cytoplasmic calcium elevation and disease resistance in rice , 2019, Cell Research.

[34]  Jonathan D. G. Jones,et al.  A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling , 2006, Science.

[35]  Qian Qian,et al.  Unravelling miRNA regulation in yield of rice (Oryza sativa) based on differential network model , 2018, Scientific Reports.

[36]  E. Peiter,et al.  Cytosolic calcium signals elicited by the pathogen-associated molecular pattern flg22 in stomatal guard cells are of an oscillatory nature. , 2014, The New phytologist.

[37]  Jian-Min Zhou,et al.  The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling , 2021, Cell.

[38]  R. Terauchi,et al.  Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. , 2012, The Plant journal : for cell and molecular biology.

[39]  T. Boller,et al.  A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. , 2009, Annual review of plant biology.

[40]  M. Zytnicki,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. , 2013, The New phytologist.

[41]  W. Karłowski,et al.  Developmental changes in barley microRNA expression profiles coupled with miRNA target analysis. , 2016, Acta biochimica Polonica.

[42]  Ping He,et al.  Differential innate immune signalling via Ca2+ sensor protein kinases , 2010, Nature.

[43]  Jing Fan,et al.  Expressing a Target Mimic of miR156fhl-3p Enhances Rice Blast Disease Resistance Without Yield Penalty by Improving SPL14 Expression , 2020, Frontiers in Genetics.

[44]  L. Yan,et al.  Osa-miR439 Negatively Regulates Rice Immunity Against Magnaporthe oryzae , 2021 .

[45]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[46]  B. San Segundo,et al.  MicroRNAs in Rice Innate Immunity , 2016, Rice.

[47]  R. Dixon,et al.  Growth-defense trade-offs and yield loss in plants with engineered cell walls. , 2021, The New phytologist.

[48]  F. Martinelli,et al.  Identification of microRNAS differentially regulated by water deficit in relation to mycorrhizal treatment in wheat , 2019, Molecular Biology Reports.

[49]  R. Zielinski.  CALMODULIN AND CALMODULIN-BINDING PROTEINS IN PLANTS. , 1998, Annual review of plant physiology and plant molecular biology.

[50]  Shuangcheng Li,et al.  miR396-OsGRFs Module Balances Growth and Rice Blast Disease-Resistance , 2019, Front. Plant Sci..

[51]  Hailing Jin,et al.  Host small RNAs are big contributors to plant innate immunity. , 2009, Current opinion in plant biology.

[52]  Xuemei Chen,et al.  The 'how' and 'where' of plant microRNAs. , 2017, The New phytologist.

[53]  H. Budak,et al.  miRNA expression patterns of Triticum dicoccoides in response to shock drought stress , 2011, Planta.

[54]  M. Yano,et al.  Two Adjacent Nucleotide-Binding Site–Leucine-Rich Repeat Class Genes Are Required to Confer Pikm-Specific Rice Blast Resistance , 2008, Genetics.

[55]  Hailing Jin,et al.  miRNA863-3p sequentially targets negative immune regulator ARLPKs and positive regulator SERRATE upon bacterial infection , 2016, Nature Communications.

[56]  Jing Fan,et al.  Osa‐miR398b boosts H2O2 production and rice blast disease‐resistance via multiple superoxide dismutases , 2019, The New phytologist.

[57]  Jing Fan,et al.  Osa-miR1873 fine-tunes rice immunity against Magnaporthe oryzae and yield traits. , 2019, Journal of integrative plant biology.

[58]  S. He,et al.  Growth-defense tradeoffs in plants: a balancing act to optimize fitness. , 2014, Molecular plant.

[59]  Jing Fan,et al.  Osa-miR169 Negatively Regulates Rice Immunity against the Blast Fungus Magnaporthe oryzae , 2017, Front. Plant Sci..

[60]  Min Shi,et al.  Identification of quantitative trait Loci for lipid metabolism in rice seeds. , 2012, Molecular plant.

[61]  Xuewei Chen,et al.  A single transcription factor promotes both yield and immunity in rice , 2018, Science.

[62]  Xiaoming Zhang,et al.  The function of small RNAs in plant biotic stress response. , 2016, Journal of integrative plant biology.

[63]  Yan Li,et al.  Identification of MicroRNAs Involved in Pathogen-Associated Molecular Pattern-Triggered Plant Innate Immunity1[W] , 2010, Plant Physiology.