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Journal of Integrative Agriculture  2026, Vol. 25 Issue (4): 1566-1574    DOI: 10.1016/j.jia.2024.08.013
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A novel effector of Aphelenchoides besseyi, AbPFN3, interacts with multiple host proteins to facilitate parasitic nematode and sustain infection in rice

Xin Huang1, 3, Yuankai Chi1, Wei Zhao1, Wenkun Huang2, Deliang Peng2#, Rende Qi1#

1 Institute of Plant Protection and Agro-products Safety, Anhui Academy of Agricultural Sciences, Hefei 230031, China

2 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

3 Institute of Plant Protection, Xinjiang Uygur Autonomous Region Academy of Agricultural Sciences, Urumqi 830091, China

 Highlights 
Identifies AbPFN3 as a novel Aphelenchoides besseyi effector upregulated in juveniles and secreted from esophageal glands.
Reveals AbPFN3 promotes parasitism by targeting host proteins (OsAAC1/OsBAP31/OsSAUR50) across multiple cellular compartments.
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摘要  

水稻干尖线虫(Aphelenchoides besseyi)可侵染水稻、大豆、棉花等多种作物,给农业生产造成严重损失。目前水稻干尖线虫效应子的研究较少,该线虫的侵染分子机制仍不明确。研究水稻干尖线虫的致病分子机理,找到致病的关键靶标,对于水稻干尖线虫绿色防控技术的开发具有重要的意义。本研究使用原位杂交、qPCRCo-IP/MSBiFC、转基因过表达等技术对水稻干尖线虫分泌的一个关键致病效应子AbPFN3的功能进行了解析。AbPFN3基因全长381 bp,编码氨基酸长度126 aa。序列分析显示,AbPFN3与马铃薯白线虫的GpPFN3的序列相似性最高,为59.52%AbPFN3具有典型的profilin蛋白结构域,但不具有信号肽和跨膜结构域。通过qPCR证实了AbPFN3在幼虫中高表达,使用原位杂交的方法得出AbPFN3是一个在食道腺特异表达的基因。亚细胞定位显示,AbPFN3被定位于内质网、叶绿体等多个细胞器上。使用Co-IP/MSpull-downBiFC等方法探究AbPFN3与寄主蛋白的互作,明确了水稻中与AbPFN3存在互作关系的蛋白有OsAAC1OsBAP31OsSAUR50,同时确定了这种互作发生在内质网、细胞质和质膜等多个细胞器中。在拟南芥中稳定表达AbPFN3基因后,植株的表型产生了明显变化,转基因拟南芥的株高显著高于野生型。在基因表达层面,转基因拟南芥中AAC1BAP31基因的表达量显著上调,相反RGA2SAUR50的表达量显著下调。综上所述,水稻干尖线虫AbPFN3是一个由食道腺分泌的效应子,与多个寄主蛋白存在互作关系,可能通过影响寄主的细胞发育、防卫反应、能量运输等过程促进水稻干尖线虫的侵染。本研究丰富了对水稻干尖线虫效应子分子互作模式的认识,证实了水稻干尖线虫的效应子可以通过与多个寄主蛋白的互作对寄主的多个生物学过程进行调控,进而促进线虫的侵染和寄生。



Abstract  

The rice white tip nematode (RWTN) Aphelenchoides besseyi secretes effectors that manipulate host plant cells to facilitate successful parasitism and sustain infection.  Although the number of identified RWTN effectors remains limited, their mechanisms of interaction with host plants are largely unknown.  Profilins (PFNs) function as molecular hubs that regulate complex interaction networks.  To advance understanding of PFN3 in plant-parasitic nematodes, we identified an effector from A. besseyi, designated AbPFN3.  AbPFN3 is transcriptionally upregulated during the juvenile stage of the nematode, and in situ hybridization localized its expression to the esophageal glands.  Three rice (Oryza sativa) proteins, ADP/ATP carrier protein 1 (OsAAC1), B-cell receptor-associated protein 31 (OsBAP31) and Small Auxin Up RNA 50 (OsSAUR50), were identified as interactors of AbPFN3, with interactions occurring in distinct cellular compartments, including the endoplasmic reticulum, cytoplasm, and plasma membrane.  Transgenic analyses revealed that AbPFN3 expression significantly increased plant height and upregulated AAC1 and BAP31, while downregulating RGA2 and SAUR50.  This study characterizes AbPFN3 as a novel effector secreted by A. besseyi that interacts with multiple host proteins, highlighting its potential role in modulating host defense responses and cell development processes.

Keywords:  Aphelenchoides besseyi       profilin 3        protein–protein interactions        effector  
Received: 20 February 2024   Accepted: 12 July 2024 Online: 22 August 2024  
Fund: 
This work was supported by the National Natural Science Foundation of China (32001881) and the National Key Research and Development Program of China (2023YFD1400400).
About author:  Xin Huang, E-mail: huangxin0924@126.com; #Correspondence Deliang Peng, E-mail: dlpeng@ippcaas.cn; Rende Qi, E-mail: rende7@126.com

Cite this article: 

Xin Huang, Yuankai Chi, Wei Zhao, Wenkun Huang, Deliang Peng, Rende Qi. 2026. A novel effector of Aphelenchoides besseyi, AbPFN3, interacts with multiple host proteins to facilitate parasitic nematode and sustain infection in rice. Journal of Integrative Agriculture, 25(4): 1566-1574.

An L, Zhang S, Guo P, Song L, Xie C, Guo H, Fang R, Jia Y. 2022. RIR1 represses plant immunity by interacting with mitochondrial complex I subunit in rice. Molecular Plant Pathology23, 92–103.

Bobay B G, DiGennaro P, Scholl E, Imin N, Djordjevic M A, Bird D M. 2013. Solution NMR studies of the plant peptide hormone CEP inform function. FEBS Letters587, 3979–3985.

De Boer J M, Yan Y, Smant G, Davis E L, Baum T J. 1998. In-situ hybridization to messenger RNA in Heterodera glycinesJournal of Nematology30, 309–312.

Chen J, Hu L, Sun L, Lin B, Huang K, Zhuo K, Liao J. 2018. A novel Meloidogyne graminicola effector, MgMO237, interacts with multiple host defence-related proteins to manipulate plant basal immunity and promote parasitism. Molecular Plant Pathology19, 1942–1955.

Chen J, Lin B, Huang Q, Hu L, Zhuo K, Liao J. 2017. A novel Meloidogyne graminicola effector, MgGPP, is secreted into host cells and undergoes glycosylation in concert with proteolysis to suppress plant defenses and promote parasitism. PLoS Pathogens13, e1006301.

Diedrich G, Spahn C M T, Stelzl U, Schäfer M A, Wooten T, Bochkariov D E, Cooperman B S, Traut R R, Nierhaus K H. 2000. Ribosomal protein L2 is involved in the association of the ribosomal subunits, tRNA binding to A and P sites and peptidyl transfer. The EMBO Journal19, 5241–5250.

Dubreuil G, Magliano M, Deleury E, Abad P, Rosso M N. 2007. Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism. New Phytologist176, 426–436.

Espada M, Eves-van den Akker S, Maier T, Vijayapalani P, Baum T, Mota M, Jones J T. 2018. STATAWAARS: A promoter motif associated with spatial expression in the major effector-producing tissues of the plant-parasitic nematode Bursaphelenchus xylophilusBMC Genomics19, 1–13.

Eves-van den Akker S, Birch P R J. 2016. Opening the effector protein toolbox for plant-parasitic cyst nematode interactions. Molecular Plant9, 1451–1453.

Eves-van den Akker S, Lilley C J, Jones J T, Urwin P E. 2014. Identification and characterisation of a hyper-variable apoplastic effector gene family of the potato cyst nematodes. PLoS Pathogens10, e1004391.

Favoreto L, Faleiro V O, Freitas M A, Brauwers L R, Galbieri R, Homiak J A, Lopes-Caitar V S, Marcelino-Guimarães F C, Meye M C. 2018. First report of Aphelenchoides besseyi infecting the aerial part of cotton plants in Brazil. Plant Disease102, 2662.

Fiore C, Trezeguet V, Le Saux A, Roux P, Schwimmer C, Dianoux A C, Noel F, Lauquin G J, Brandolin G, Vignais P V. 1998. The mitochondrial ADP/ATP carrier: Structural, physiological and pathological aspects. Biochemie80, 137–150.

Fu J, Momčilović I, Prasad P V. 2012. Roles of protein synthesis elongation factor EF-Tu in heat tolerance in plants. Journal of Botany, 2012, 835836.

Halperin T, Zheng B, Itzhaki H, Clarke A K, Adam Z. 2001. Plant mitochondria contain proteolytic and regulatory subunits of the ATP-dependent Clp protease. Plant Molecular Biology45, 461–468.

He F, Chen S, Ning Y, Wang G L. 2016. Rice (Oryza sativa) protoplast isolation and its application for transient expression analysis. Current Protocols in Plant Biology1, 373–383.

Huang X, Chi Y K, Birhan A A, Zhao W, Qi R D, Peng D L. 2022. The new effector AbSCP1 of foliar nematode (Aphelenchoides besseyi) is required for parasitism rice. Journal of Integrative Agriculture21, 1084–1093.

Huang X, Xu C L, Yang S H, Li J Y, Wang H L, Zhang Z X, Chen C, Xie H. 2019. Life-stage specifc transcriptomes of a migratory endoparasitic plant nematode, Radopholus similis elucidate a diferent parasitic and life strategy of plant parasitic nematodes. Scientific Reports9, 6277.

Jaouannet M, Magliano M, Arguel M J, Gourgues M, Evangelisti E, Abad P, Rosso M N. 2013. The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Molecular Plant-Microbe Interactions26, 97–105.

Jaubert S, Laffaire J B, Ledger T N, Escoubas P, Amri E Z, Abad P, Rosso M N. 2004. Comparative analysis of two 14-3-3 homologues and their expression pattern in the root-knot nematode Meloidogyne incognitaInternational Journal for Parasitology34, 873–880.

Ji H, Xie J, Han Z. Yang F, Yu W, Peng Y, Qing X. 2023. Complete genome sequencing of nematode Aphelenchoides besseyi, an economically important pest causing rice white-tip disease. Phytopathology Research5, 1–13.

Kim J, Yang R, Chang C, Park Y, Tucker M L. 2018. The root-knot nematode Meloidogyne incognita produces a functional mimic of the Arabidopsis INFLORESCENCE DEFICIENT IN ABSCISSION signaling peptide. Journal of Experimental Botany69, 3009–3021.

Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution33, 1870–1874.

Lambert K N, Allen K D, Sussex I M. 1999. Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanicaMolecular Plant-Microbe Interactions12, 328–336.

Leelarasamee N, Zhang L, Gleason C. 2018. The root-knot nematode effector MiPFN3 disrupts plant actin filaments and promotes parasitism. PloS Pathogens14, e1006947.

Lilley C J, Maqbool A, Wu D, Yusup H B, Jones L M, Birch P R J, Banfield M J, Urwin P E, Eves-van den Akker S. 2018. Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene. PLoS Genetics14, e1007310.

Lin B, Zhuo K, Chen S, Hu L, Sun L, Wang X, Zhang L, Liao J. 2016. A novel nematode effector suppresses plant immunity by activating host reactive oxygen species-scavenging system. New Phytologist209, 1159–1173.

Lin B, Zhuo K, Wu P, Cui R, Zhang L, Liao J. 2013. A novel effector protein, MJ-NULG1a, targeted to giant cell nuclei plays a role in Meloidogyne javanica parasitism. Molecular Plant-Microbe Interactions26, 55–66.

Palomares-Rius J E, Hirooka Y, Tsai I J, Masuya H, Hino A, Kanzaki N, Kikuchi T. 2014. Distribution and evolution of glycoside hydrolase family 45 cellulases in nematodes and fungi. BMC Evolutionary Biology14, 69.

Masonbrink R, Maier T R, Muppirala U, Seetharam A S, Lord E, Juvale P S, Schmutz J, Johnson N T, Korkin D, Mitchum M G, Mimee B, Eves-van den Akker S, Hudson M, Severin A J, Baum T J. 2019. The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes. BMC Genomics20, 1–14.

Meyer M C, Favoreto L, Klepker D, Marcelino-Guimarães F C. 2017. Soybean green stem and foliar retention syndrome caused by Aphelenchoides besseyiTropical Plant Pathology42, 403–409.

Mishal R, Luna-Arias J P. 2022. Role of the TATA-box binding protein (TBP) and associated family members in transcription regulation. Gene833, 146581.

Mitchum M G, Wang X, Wang J, Davis E L. 2012. Role of nematode peptides and other small molecules in plant parasitism. Annual Review of Phytopathology50, 175–195.

van Mourik H, van Dijk A D J, Stortenbeker N, Angenent G C, Bemer M. 2017. Divergent regulation of Arabidopsis SAUR genes: A focus on the SAUR10-clade. BMC Plant Biology17, 1–14.

Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, Bielach A, Petrášek J, Zhang J, Gaykova V, Stierhof Y D, Dobrev P , Schwarzerová K, Rolčík J, Seifertová D, Luschnig C, Benková E, Zažímalová E, Geisler M, Friml J. 2009. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature459, 1136–1140.

Pankratenko A V, Atabekova A K, Lazareva E A, Baksheeva V E, Zhironkina O A, Zernii E Y, Owens R A, Solovyev A G, Morozov S Y. 2017. Plant-specific 4/1 polypeptide interacts with an endoplasmic reticulum protein related to human BAP31. Planta245, 193–205.

Pogorelko G, Juvale P S, Rutter W B, Hewezi T, Hussey R, Davis E L, Mitchum M G, Baum T J. 2016. A cyst nematode effector binds to diverse plant proteins, increases nematode susceptibility and affects root morphology. Molecular Plant Pathology17, 832–844.

Postma W J, Slootweg E J, Rehman S, Finkers-Tomczak A, Tytgat T O G, van Gelderen K, Lozano-Torres J L, Roosien J, Pomp R, van Schaik C, Bakker J, Goverse A, Smant G. 2012. The effector SPRYSEC-19 of Globodera rostochiensis suppresses CC-NB-LRR-mediated disease resistance in plants. Plant Physiology160, 944–954.

Quistgaard E M. 2021. BAP31: Physiological functions and roles in disease. Biochimie186, 105–129.

Rutter W B, Hewezi T, Maier T R, Mitchum M G, Davis E L. Hussey R S. Baum T J. 2014. Members of the Meloidogyne avirulence protein family contain multiple plant ligand-like motifs. Phytopathology104, 879–885.

Siddique S, Radakovic Z S, De La Torre C M, Chronis D, Novák O, Ramireddy E, Holbein J, Matera C, Hütten M, Gutbrod P, Anjam M S, Rozanska E, Habash S, Elashry A, Sobczak M, Kakimoto T, Strnad M, Schmülling T, Mitchum M G, Grundler F M W. 2015. A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants. Proceedings of the National Academy of Sciences of the United States of America112, 12669–12674.

Silverstone A L, Jung H S, Dill A, Kawaide H, Kamiya Y, Sun T P. 2001. Repressing a repressor: Gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. The Plant Cell13, 1555–1566.

Song H, Lin B, Huang Q, Sun L, Chen J, Hu L, Zhuo K, Liao J. 2021. The Meloidogyne graminicola effector MgMO289 targets a novel copper metallochaperone to suppress immunity in rice. Journal of Experimental Botany72, 5638–5655.

Sukarta O C A, Zheng Q, Slootweg E J, Mekken M, Mendel M, Putker V, Bertran A, Brand A, Overmars H, Pomp R, Roosien J, Boeren S, Smant G, Goverse A. 2022. GLYCINE-RICH RNA-BINDING PROTEIN 7 potentiates effector-triggered immunity through an RNA recognition motif. Plant Physiology189, 972–987.

Sun N, Wang J, Gao Z, Dong J, He H, Terzaghi W, Wei N, Deng X W, Chen H. 2016. Arabidopsis SAURs are critical for differential light regulation of the development of various organs. Proceedings of the National Academy of Sciences of the United States of America113, 6071–6076.

Tang J, Xia H, Cao M, Zhang X, Zeng W, Hu S, Tong W, Wang J, Wang J, Yu J, Yang H, Zhu L. 2004. A comparison of rice chloroplast genomes. Plant Physiology135, 412–420.

Tucker M L, Yang R. 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. Experimental Parasitology134, 165–170.

Tulek A, Kepenekci I, Cobanoglu S, Hekimhan H, Devran Z, Melik B, Elekcioglu H I. 2009. A new culturing method for the rice white tip nematode, Aphelenchoides besseyi Christie, 1942, on carrot discs. Russian Journal of Nematology17, 135–136.

Vieira P, Danchin E G J, Neveu C, Crozat C, Jaubert S, Hussey R S, Engler G, Abad P, de Almeida-Engler J, Castagnone-Sereno P, Rosso M. 2011. The plant apoplasm is an important recipient compartment for nematode secreted proteins. Journal of Experimental Botany62, 1241–1253.

Wang D W, Xu C L, Ding S W, Huang X, Cheng X, Zhang C, Chen C, Xie H. 2018. Identification and function of FAR protein family genes from a transcriptome analysis of Aphelenchoides besseyiBioinformatics34, 2936–2943.

Wei H, Wang X, He Y, Xu H, Wang L. 2021. Clock component OsPRR73 positively regulates rice salt tolerance by modulating OsHKT2;1-mediated sodium homeostasis. The EMBO Journal40, e105086.

Witke W. 2004. The role of profilin complexes in cell motility and other cellular processes. Trends in Cell Biology14, 461–469.

Yang S, Li J, Yang S, Tang S, Wang H, Xu C, Xie H. 2024. A chorismate mutase from Radopholus similis plays an essential role in pathogenicity. Journal of Integrative Agriculture23, 923–937.

Zhang H, Yu Z, Yao X, Chen J, Chen X, Zhou H, Lou Y, Ming Feng, Jin Y. 2021. Genome-wide identification and characterization of small auxin-up RNA (SAUR) gene family in plants: Evolution and expression profiles during normal growth and stress response. BMC Plant Biology21, 1–14.

Zhang X, Peng H, Zhu S, Xing J, Li X, Zhu Z, Zheng J, Wang L, Wang B, Chen J, Ming Z, Yao K, Jian J, Luan S, Coleman-Derr D, Liao H, Peng Y, Peng D, Yu F. 2020. Nematode-encoded RALF peptide mimics facilitate parasitism of plants through the FERONIA receptor kinase. Molecular Plant13, 1434–1454.

Zhao J, Duan Y, Kong L A, Huang W K, Peng D L, Liu S M. 2022. Opposite beet Cyst nematode-infection phenotypes of transgenic Arabidopsis between overexpressing GmSNAP18 and AtSNAP2 and between overexpressing GmSHMT08 and AtSHMT4. Phytopathology112, 2383–2390.

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