Nematode-Encoded RALF Peptide Mimics Facilitate Parasitism of Plants through the FERONIA Receptor Kinase

Abad, 2008, Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita, Nat. Biotechnol., 26, 909, 10.1038/nbt.1482 Altschul, 1990, Basic local alignment search tool, J. Mol. Biol., 215, 403, 10.1016/S0022-2836(05)80360-2 Atkinson, 2013, Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses, Plant Physiol., 162, 2028, 10.1104/pp.113.222372 Blackburn, 2020, Twenty years of progress in physiological and biochemical investigation of RALF peptides, Plant Physiol., 182, 1657, 10.1104/pp.19.01310 Bobay, 2013, Solution NMR studies of the plant peptide hormone CEP inform function, FEBS Lett., 587, 3979, 10.1016/j.febslet.2013.10.033 Bostock, 2005, Signal crosstalk and induced resistance: straddling the line between cost and benefit, Annu. Rev. Phytopathol., 43, 545, 10.1146/annurev.phyto.41.052002.095505 Campbell, 2017, A comprehensive analysis of RALF proteins in green plants suggests there are two distinct functional groups, Front. Plant Sci., 8, 37, 10.3389/fpls.2017.00037 Cao, 2012, Evolution of the RALF gene family in plants: gene duplication and selection patterns, Evol. Bioinform., 8, 271, 10.4137/EBO.S9652 Chakravorty, 2018, A kinase-dead version of FERONIA receptor-like kinase has dose-dependent impacts on rosette morphology and RALF1-mediated stomatal movements, FEBS Lett., 592, 3429, 10.1002/1873-3468.13249 Chen, 2016, FERONIA interacts with ABI2-type phosphatases to facilitate signaling cross-talk between abscisic acid and RALF peptide in Arabidopsis, Proc. Natl. Acad. Sci. U S A, 113, E5519, 10.1073/pnas.1608449113 Chen, 2020, FERONIA cytoplasmic domain: node of varied signal outputs, aBIOTECH, 1, 135, 10.1007/s42994-020-00017-y de Boer, 1999, Developmental expression of secretory beta-1,4 endoglucanases in the subventral esophageal glands of Heterodera glycines, Mol. Plant Microbe Interact., 12, 663, 10.1094/MPMI.1999.12.8.663 Dong, 2019, FERONIA regulates auxin-mediated lateral root development and primary root gravitropism, FEBS Lett., 593, 97, 10.1002/1873-3468.13292 Doyle, 2002, Cloning and characterization of an esophageal-gland-specific pectate lyase from the root-knot nematode Meloidogyne javanica, Mol. Plant Microbe Interact., 15, 549, 10.1094/MPMI.2002.15.6.549 Doyle, 2003, Meloidogyne javanica chorismate mutase 1 alters plant cell development, Mol. Plant Microbe Interact., 16, 123, 10.1094/MPMI.2003.16.2.123 Du, 2016, Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis, Proc. Natl. Acad. Sci. U S A, 113, E8326, 10.1073/pnas.1609626113 Duan, 2014, Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis, Nat. Commun., 5, 4129, 10.1038/ncomms4129 Duan, 2010, FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development, Proc. Natl. Acad. Sci. U S A, 107, 17821, 10.1073/pnas.1005366107 Dünser, 2019, Extracellular matrix sensing by FERONIA and leucine-rich repeat extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana, EMBO J., 38, e100353, 10.15252/embj.2018100353 Eisenback, 2009, General morphology, 18 Emsley, 2004, Coot: model-building tools for molecular graphics, Acta Crystallogr. D Biol. Crystallogr., 60, 2126, 10.1107/S0907444904019158 Escobar-Restrepo, 2007, The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception, Science, 317, 656, 10.1126/science.1143562 Eulgem, 2007, Networks of WRKY transcription factors in defense signaling, Curr. Opin. Plant Biol., 10, 366, 10.1016/j.pbi.2007.04.020 Feng, 2019, LORELEI-LIKE GPI-ANCHORED PROTEINS 2/3 regulate pollen tube growth as chaperones and coreceptors for ANXUR/BUPS receptor kinases in Arabidopsis, Mol. Plant, 12, 1612, 10.1016/j.molp.2019.09.004 Feng, 2018, The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling, Curr. Biol., 28, 666, 10.1016/j.cub.2018.01.023 Franck, 2018, Plant malectin-like receptor kinases: from cell wall integrity to immunity and beyond, Annu. Rev. Plant Biol., 69, 301, 10.1146/annurev-arplant-042817-040557 Fukao, 2004, Plant responses to hypoxia—is survival a balancing act?, Trends Plant Sci., 9, 449, 10.1016/j.tplants.2004.07.005 Ge, 2017, Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling, Science, 358, 1596, 10.1126/science.aao3642 Ge, 2019, How CrRLK1L receptor complexes perceive RALF signals, Trends Plant Sci., 24, 978, 10.1016/j.tplants.2019.09.002 Ge, 2019, LLG2/3 are co-receptors in BUPS/ANX-RALF signaling to regulate Arabidopsis pollen tube integrity, Curr. Biol., 29, 3256, 10.1016/j.cub.2019.08.032 Gonneau, 2018, Receptor kinase THESEUS1 is a rapid alkalinization factor 34 receptor in Arabidopsis, Curr. Biol., 28, 2452, 10.1016/j.cub.2018.05.075 Gonzali, 2015, Universal stress protein HRU1 mediates ROS homeostasis under anoxia, Nat. Plants, 1, 15151, 10.1038/nplants.2015.151 Grundler, 1998, Formation of wall openings in root cells of Arabidopsis thaliana following infection by the plant-parasitic nematode Heterodera schachtii, Eur. J. Plant Pathol., 104, 545, 10.1023/A:1008692022279 Guo, 2018, FERONIA receptor kinase contributes to plant immunity by suppressing jasmonic acid signaling in Arabidopsis thaliana, Curr. Biol., 28, 3316, 10.1016/j.cub.2018.07.078 Hansen, 2019, FERONIA mutation induces high levels of chloroplast-localized Arabidopsides which are involved in root growth, Plant J., 97, 341, 10.1111/tpj.14123 Harris, 2020, WormBase: a modern model organism information resource, Nucleic Acids Res., 48, D762 Haruta, 2014, A peptide hormone and its receptor protein kinase regulate plant cell expansion, Science, 343, 408, 10.1126/science.1244454 Hewezi, 2008, Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism, Plant Cell, 20, 3080, 10.1105/tpc.108.063065 Hewezi, 2015, The cyst nematode effector protein 10A07 targets and recruits host posttranslational machinery to mediate its nuclear trafficking and to promote parasitism in Arabidopsis, Plant Cell, 27, 891, 10.1105/tpc.114.135327 Hofte, 2015, The yin and yang of cell wall integrity control: brassinosteroid and FERONIA signaling, Plant Cell Physiol., 56, 224, 10.1093/pcp/pcu182 Huang, 2006, Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene, Proc. Natl. Acad. Sci. U S A, 103, 14302, 10.1073/pnas.0604698103 Huguet-Tapia, 2012, Draft genome sequence of Streptomyces acidiscabies 84-104, an emergent plant pathogen, J. Bacteriol., 194, 1847, 10.1128/JB.06767-11 Iberkleid, 2013, Fatty acid-and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes, PLoS One, 8, e64586, 10.1371/journal.pone.0064586 Ibrahim, 1973, Host parasite relationship of Meloidogyne incognita (Kofoid et White) Chitw. on rice, Nematol. Mediterr., 1, 8 Jones, 2006, The plant immune system, Nature, 444, 323, 10.1038/nature05286 Katoh, 2013, MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol. Biol. Evol., 30, 772, 10.1093/molbev/mst010 Keinath, 2010, PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity, J. Biol. Chem., 285, 39140, 10.1074/jbc.M110.160531 Kessler, 2010, Conserved molecular components for pollen tube reception and fungal invasion, Science, 330, 968, 10.1126/science.1195211 Kikuchi, 2017, Genome evolution of plant-parasitic nematodes, Annu. Rev. Phytopathol., 55, 333, 10.1146/annurev-phyto-080516-035434 Kyndt, 2014, Plant-parasitic nematode infections in rice: molecular and cellular insights, Annu. Rev. Phytopathol., 52, 135, 10.1146/annurev-phyto-102313-050111 Lee, 2020, Regulation of reactive oxygen species during plant immunity through phosphorylation and ubiquitination of RBOHD, Nat. Commun., 11, 1838, 10.1038/s41467-020-15601-5 Li, 2018, EBP1 nuclear accumulation negatively feeds back on FERONIA-mediated RALF1 signaling, PLoS Biol., 16, e2006340, 10.1371/journal.pbio.2006340 Li, 2016, Two FERONIA-like receptor (FLR) genes are required to maintain architecture, fertility, and seed yield in rice, Mol. Breed., 36, 151, 10.1007/s11032-016-0580-x Li, 2016, FERONIA and her pals: functions and mechanisms, Plant Physiol., 171, 2379, 10.1104/pp.16.00667 Li, 2015, Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis, Elife, 4, e06587, 10.7554/eLife.06587 Lin, 2016, A novel nematode effector suppresses plant immunity by activating host reactive oxygen species-scavenging system, New Phytol, 209, 1159, 10.1111/nph.13701 Liu, 2011, A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor, Cell Host Microbe, 9, 137, 10.1016/j.chom.2011.01.010 Lee, 2011, The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development, Plant Physiol, 155, 866, 10.1104/pp.110.167197 Majda, 2018, The role of auxin in cell wall expansion, Int. J. Mol. Sci., 19, 951, 10.3390/ijms19040951 Martinez-Medina, 2017, Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita, New Phytol., 213, 1363, 10.1111/nph.14251 Masachis, 2016, A fungal pathogen secretes plant alkalinizing peptides to increase infection, Nat. Microbiol., 1, 16043, 10.1038/nmicrobiol.2016.43 Mecchia, 2017, RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis, Science, 358, 1600, 10.1126/science.aao5467 Mendy, 2017, Arabidopsis leucine-rich repeat receptor-like kinase NILR1 is required for induction of innate immunity to parasitic nematodes, PLoS Pathog, 13, 10.1371/journal.ppat.1006284 Mitchum, 2012, Role of nematode peptides and other small molecules in plant parasitism, Annu. Rev. Phytopathol., 50, 175, 10.1146/annurev-phyto-081211-173008 Murphy, 2014, Understanding the RALF family: a tale of many species, Trends Plant Sci., 19, 664, 10.1016/j.tplants.2014.06.005 Murphy, 2012, Small signaling peptides in Arabidopsis development: how cells communicate over a short distance, Plant Cell, 24, 3198, 10.1105/tpc.112.099010 Nahar, 2011, The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice, Plant Physiol., 157, 305, 10.1104/pp.111.177576 2018, Database resources of National Center for Biotechnology information, Nucleic Acids Res., 46, D8, 10.1093/nar/gkx1095 Nguyen, 2018, A root-knot nematode small glycine and cysteine-rich secreted effector, MiSGCR1, is involved in plant parasitism, New Phytol., 217, 687, 10.1111/nph.14837 Pearce, 2001, RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development, Proc. Natl. Acad. Sci. U S A, 98, 12843, 10.1073/pnas.201416998 Pearce, 2010, Structure-activity studies of RALF, rapid alkalinization factor, reveal an essential-YISY-motif, Peptides, 31, 1973, 10.1016/j.peptides.2010.08.012 Price, 2010, FastTree 2-approximately maximum-likelihood trees for large alignments, PLoS One, 5, e9490, 10.1371/journal.pone.0009490 Prior, 2001, A surface-associated retinol-and fatty acid-binding protein (Gp-FAR-1) from the potato cyst nematode Globodera pallida: lipid binding activities, structural analysis and expression pattern, Biochem. J., 356, 387, 10.1042/bj3560387 Qi, 2015, Regulation of jasmonate-induced leaf senescence by antagonism between bHLH subgroup IIIe and IIId factors in Arabidopsis, Plant Cell, 27, 1634, 10.1105/tpc.15.00110 Replogle, 2011, Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE, Plant J., 65, 430, 10.1111/j.1365-313X.2010.04433.x Rosso, 2009, RNAi and functional genomics in plant parasitic nematodes, Annu. Rev. Phytopathol., 47, 207, 10.1146/annurev.phyto.112408.132605 Rotman, 2008, A dialogue between the SIRENE pathway in synergids and the fertilization independent seed pathway in the central cell controls male gamete release during double fertilization in Arabidopsis, Mol. Plant, 1, 659, 10.1093/mp/ssn023 Rutter, 2014, Mining novel effector proteins from the esophageal gland cells of Meloidogyne incognita, Mol. Plant Microbe Interact., 27, 965, 10.1094/MPMI-03-14-0076-R Shen, 2017, Arabidopsis glycosylphosphatidylinositol-anchored protein LLG1 associates with and modulates FLS2 to regulate innate immunity, Proc. Natl. Acad. Sci. U S A, 114, 5749, 10.1073/pnas.1614468114 Shi, 2018, The dynamics of root cap sloughing in Arabidopsis is regulated by peptide signalling, Nat. Plants, 4, 596, 10.1038/s41477-018-0212-z Shih, 2014, The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings, Curr. Biol., 24, 1887, 10.1016/j.cub.2014.06.064 Shiu, 2001, Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases, Proc. Natl. Acad. Sci. U S A, 98, 10763, 10.1073/pnas.181141598 Sindhu, 2009, Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success, J. Exp. Bot., 60, 315, 10.1093/jxb/ern289 Stegmann, 2017, The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling, Science, 355, 287, 10.1126/science.aal2541 Sun, 2018, AtrbohD functions downstream of ROP2 and positively regulates waterlogging response in Arabidopsis, Plant Signal. Behav., 13, e1513300, 10.1080/15592324.2018.1513300 Tang, 2017, Receptor kinases in plant-pathogen interactions: more than pattern recognition, Plant Cell, 29, 618, 10.1105/tpc.16.00891 Teixeira, 2016, Root-knot nematodes induce pattern-triggered immunity in Arabidopsis thaliana roots, New Phytol, 211, 276, 10.1111/nph.13893 Thynne, 2017, Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides, Mol. Plant Pathol., 18, 811, 10.1111/mpp.12444 Trapnell, 2012, Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks, Nat. Protoc., 7, 562, 10.1038/nprot.2012.016 Tsai, 2019, Regulation of root-knot nematode behavior by seed-coat mucilage-derived attractants, Mol. Plant, 12, 99, 10.1016/j.molp.2018.11.008 Tucker, 2013, A gene encoding a peptide with similarity to the plant IDA signaling peptide (AtIDA) is expressed most abundantly in the root-knot nematode (Meloidogyne incognita) soon after root infection, Exp. Parasitol., 134, 165, 10.1016/j.exppara.2013.03.019 Vieira, 2019, Plant-parasitic nematode effectors-insights into their diversity and new tools for their identification, Curr. Opin. Plant Biol., 50, 37, 10.1016/j.pbi.2019.02.007 Wang, 2019, Systemic root-shoot signaling drives jasmonate-based root defense against nematodes, Curr. Biol., 29, 1, 10.1016/j.cub.2019.08.049 Wang, 2020, Receptor kinase FERONIA regulates flowering time in Arabidopsis, BMC Plant Biol., 20, 26, 10.1186/s12870-019-2223-y Wang, 2020, RALF1-FERONIA complex affects splicing dynamics to modulate stress responses and growth in plants, Sci. Adv., 6, eaaz1622, 10.1126/sciadv.aaz1622 Wang, 1999, In planta localization of a β-1,4-endoglucanase secreted by Heterodera glycines, Mol. Plant Microbe Interact., 12, 64, 10.1094/MPMI.1999.12.1.64 Wang, 2005, A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana, Mol. Plant Pathol., 6, 187, 10.1111/j.1364-3703.2005.00270.x Wang, 2018, A novel Meloidogyne incognita chorismate mutase effector suppresses plant immunity by manipulating the salicylic acid pathway and functions mainly during the early stages of nematode parasitism, Plant Pathol., 67, 1436, 10.1111/ppa.12841 Wong, 2007, Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension, Plant Cell, 19, 4022, 10.1105/tpc.107.055624 Wu, 2007, NaRALF, a peptide signal essential for the regulation of root hair tip apoplastic pH in Nicotiana attenuata, is required for root hair development and plant growth in native soils, Plant J., 52, 877, 10.1111/j.1365-313X.2007.03289.x Xiao, 2019, Mechanisms of RALF peptide perception by a heterotypic receptor complex, Nature, 572, 270, 10.1038/s41586-019-1409-7 Xu, 2019, FERONIA phosphorylates E3 ubiquitin ligase ATL6 to modulate the stability of 14-3-3 proteins in plant C/N responses, J. Exp. Bot., 70, 6375, 10.1093/jxb/erz378 Yadav, 2006, Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection, Mol. Biochem. Parasitol., 148, 219, 10.1016/j.molbiopara.2006.03.013 Yang, 2015, Receptor protein kinase FERONIA controls leaf starch accumulation by interacting with glyceraldehyde-3-phosphate dehydrogenase, Biochem. Biophys. Res. Commun., 465, 77, 10.1016/j.bbrc.2015.07.132 Yang, 2020, Mutations of two FERONIA-like receptor genes enhance rice blast resistance without growth penalty, J. Exp. Bot., 71, 2112, 10.1093/jxb/erz541 Yu, 2014, FERONIA receptor kinase controls seed size in Arabidopsis thaliana, Mol. Plant, 7, 920, 10.1093/mp/ssu010 Yu, 2012, FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase, Proc. Natl. Acad. Sci. U S A, 109, 14693, 10.1073/pnas.1212547109 Zhang, 2020, RALF-FERONIA signaling: linking plant immune response with cell growth, Plant Commun, 1, 100084, 10.1016/j.xplc.2020.100084 Zhu, 2019, A MAPK cascade downstream of IDA-HAE/HSL2 ligand-receptor pair in lateral root emergence, Nat. Plants, 5, 414, 10.1038/s41477-019-0396-x Zhu, 2020, The RALF1-FERONIA complex phosphorylates eIF4E1 to promote protein synthesis and polar root hair growth, Mol. Plant, 13, 698, 10.1016/j.molp.2019.12.014