Advances of LORELEI-like Glycosylphosphatidylinositol-anchor (LLG) Proteins in Plants

doi:10.11983/CBB20058

Abstract

Abstract: The outer surface of plasma membrane (PM)-localized LORELEI-like glycosylphosphatidylinositol-anchor (LLG) proteins, as the molecular chaperone of CrRLK1Ls family of receptor-like kinase, are involved in the transport of CrRLKs and extracellular signal transduction, regulating plant reproduction, development, as well as immune and stress responses. LLG2/3 interacting with ANX and BUPS regulates pollen tube growth and rupture. LLG1 interacted with FER activates the ROPGEF1-ROP2-NADPH oxidase pathway for ROS production, and then promotes root cell elongation and root hair growth. Besides, LLG1, as co-receptor of FER, interacts with RALFs, and then regulates G protein β (AGB1), PM H ⁺-ATPase activity, as well as the homeostasis of intracellular ROS and Ca ²⁺, for modulating stomata and roots in response to salinity. For immune response, LLG1 interacts with FLS2 and EFR, activating the downstream RbohD for ROS production. This review provides important information for understanding LLG biological functions.

Key words: LLG, RALF, pollen tube, root, immune and salinity responses

Sijia Li, Yongxue Zhang, Mingsheng Jia, Ying Li, Shaojun Dai. Advances of LORELEI-like Glycosylphosphatidylinositol-anchor (LLG) Proteins in Plants[J]. Chinese Bulletin of Botany, 2020, 55(5): 541-550.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.chinbullbotany.com/EN/10.11983/CBB20058

https://www.chinbullbotany.com/EN/Y2020/V55/I5/541

Figures/Tables 2

Figure 1 Arabidopsis LLG amino acid sequences and 3D structure model (A) LLG amino acid sequence (The colored boxes indicate the N-terminal signal peptide, sequence conservative frame, C-terminal conformational flexible region, and C-terminal GPI anchor region, respectively; the triangles, green dots, diamonds and pentagonal stars represent 8 Cys sites that can form 4 pairs of disulfide bonds, and the blue dots represent conservative amino acid sites); (B) The 3D structure of amino acids 46-138 of LLG1 (α-helix, β-sheet, N terminal (46), C terminal (138), and conserved 8 Cys sites formed 4 pairs of disulfide bonds)

Figure 2 Interaction between different members of the LLG and RLK family proteins regulates pollen and root development and salt and immune response processes (A) LLG2/3 interacts with ANX1/2 and BUPS1/2 to regulate pollen tube growth and burst; (B) LLG1 interacts with FER to regulate root and root hair growth; (C) LLG1 interacts with FER to regulate salt stress response; (D) LLG1 interacts with FLS2 and EFR to regulate the immune response. ABA: Abscisic acid; ABI2: ABA insensitive 2; AGB1: Heterotrimeric G-protein β-subunit; AHA2: Plasma membrane H+-ATPase 2; ANX1/2: ANXUR1/2; BAK1: Brassinosteroid insensitive 1-associated receptor kinase 1; BIK1: Botrytis-induced kinase 1; BUPS1/2: Buddha’s paper seal1/2; ECD: Extracellular domain; EDR1: Enhanced disease resistance 1; EFR: EF-Tu receptor; elf18: 18 amino acid peptide of EF-Tu N-terminus; eXJM: Extracellular membrane domain; FER: FERONIA; flg22: 22 amino acid peptide of bacterial flagellin N-terminus; FLS2: Flagellin sensing 2; GDP: Guanosine diphosphate; GEF1/4/10: Guanine nucleotide exchange factor1/4/10; GTP: Guanosine triphosphate; KD: Kinase domain; LLG1/2/3: LORELEI-like GPI-anchored protein1/2/3; LRR: Leucine-rich repeat; LRX: Leucine-rich repeat extensin-like protein; MAPK: Mitogen-activated protein kinase; MKK: Mitogen-activated protein kinase kinase; MLD: Malectin-like domain; NSCC: Non-selective cation channels; PR1: Pathogenesis-related factor 1; RALF: Rapid alkalinization factor; Rboh: Respiratory burst oxidase homolog; ROP1/11: Rho-related GTPase1/11 from plants; S1P: Site-1 protease; SLAC1: Slow anion channel 1; SnRK2: Serine/threonine-protein kinase SnRK2D; TM: Transmembrane domain. The solid line represents the direct regulation process, the dotted line represents the indirect regulation process or material transport. The arrow represents promotion, and the T represents inhibition.

References 50

[1]	Chen J, Yu F, Liu Y, Du CQ, Li XS, Zhu SR, Wang XC, Lan WZ, Rodriguez PL, Liu XM, Li DP, Chen LB, Luan S ( 2016). FERONIA interacts with ABI2-type phosphatases to facilitate signaling cross-talk between abscisic acid and RALF peptide in Arabidopsismodification. Proc Natl Acad Sci USA 113, E5519-E5527. DOI URL PMID
[2]	Cheung AY, Li C, Zou YJ, Wu HM ( 2014). Glycosylphosphatidylinositol anchoring: control through modification. Plant Physiol 166, 748-750. DOI URL PMID
[3]	Deslauriers SD, Larsen PB ( 2010). FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Mol Plant 3, 626-640. URL PMID
[4]	Dinneny JR, Long TA, Wang JY, Jung JW, Mace D, Pointer S, Barron C, Brady SM, Schiefelbein J, Benfey PN ( 2008). Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320, 942-945. DOI URL PMID
[5]	Duan QH, Kita D, Johnson EA, Aggarwal M, Gates L, Wu HM, Cheung AY ( 2014). Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun 5, 3129. DOI URL PMID
[6]	Duan QH, Kita D, Li C, Cheung AY, Wu HM ( 2010). FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc Natl Acad Sci USA 107, 17821-17826. DOI URL PMID
[7]	Duan QH, Liu MCJ, Kita D, Jordan SS, Yeh FLJ, Yvon R, Carpenter H, Federico AN, Garcia-Valencia LE, Eyles SJ, Wang CS, Wu HM, Cheung AY ( 2020). FERONIA controls pectin- and nitric oxide-mediated male-female interaction. Nature 579, 561-566. URL PMID
[8]	Feng HQ, Liu C, Fu R, Zhang MM, Li H, Shen LP, Wei QQ, Sun X, Xu L, Ni B, Li C ( 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, 1612-1623. DOI URL PMID
[9]	Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan QH, Liu MC, Maman J, Steinhorst L, Schmitz- Thom I, Yvon R, Kudla J, Wu HM, Cheung AY, Dinneny JR ( 2018). The FERONIA receptor kinase maintains cell- wall integrity during salt stress through Ca ²+ signaling . Curr Biol 28, 666-675. DOI URL PMID
[10]	Franck CM, Westermann J, Boisson-Dernier A ( 2018). Plant malectin-like receptor kinases: from cell wall integrity to immunity and beyond. Annu Rev Plant Biol 69, 301-328. DOI URL PMID
[11]	Frye CA, Tang DZ, Innes RW ( 2001). Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci USA 98, 373-378. DOI URL PMID
[12]	Ge ZX, Bergonci T, Zhao YL, Zou YJ, Du S, Liu MC, Luo XJ, Ruan H, García-Valencia LE, Zhong S, Hou SY, Huang QP, Lai LH, Moura DS, Gu HY, Dong J, Wu HM, Dresselhaus T, Xiao JY, Cheung AY, Qu LJ ( 2017). Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358, 1596-1600. DOI URL PMID
[13]	Ge ZX, Cheung AY, Qu LJ ( 2019). Pollen tube integrity regulation in flowering plants: insights from molecular assemblies on the pollen tube surface. New Phytol 222, 687-693. DOI URL PMID
[14]	Guo HQ, Li L, Ye HX, Yu XF, Algreen A, Yin YH ( 2009). Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci USA 106, 7648-7653. DOI URL PMID
[15]	Haruta M, Monshausen G, Gilroy S, Sussman MR ( 2008). A cytoplasmic Ca ²+ functional assay for identifying and purifying endogenous cell signaling peptides in Arabidopsis seedlings: identification of AtRALF1 peptide. Biochemistry 47, 6311-6321. DOI URL PMID
[16]	Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR ( 2014). A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343, 408-411. DOI URL PMID
[17]	Hou YN, Guo XY, Cyprys P, Zhang Y, Bleckmann A, Cai L, Huang QP, Luo Y, Gu HY, Dresselhaus T, Dong J, Qu LJ ( 2016). Maternal ENODLs are required for pollen tube reception in Arabidopsis. Curr Biol 26, 2343-2350. DOI URL PMID
[18]	Huang GQ, Li E, Ge FR, Li S, Wang Q, Zhang CQ, Zhang Y ( 2013). Arabidopsis RopGEF4 and RopGEF10 are important for FERONIA-mediated developmental but not environmental regulation of root hair growth. New Phytol 200, 1089-1101. DOI URL PMID
[19]	Johnson MA, Harpe JF, Palanivelu R ( 2019). A fruitful journey: pollen tube navigation from germination to fertilization. Annu Rev Plant Biol 70, 809-837. URL PMID
[20]	José-Estanyol M, Gomis-Rüth FX, Puigdomènech P ( 2004). The eight-cysteine motif, a versatile structure in plant proteins. Plant Physiol Biochem 42, 355-365. DOI URL PMID
[21]	Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazaki T, Senzaki E, Hamamura Y, Higashiyama T, Takayama S, Abe M, Kuchitsu K ( 2014). Ca²⁺-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26, 1069-1080. DOI URL PMID
[22]	Keinath NF, Kierszniowska S, Lorek J, Bourdais G, Kessler SA, Shimosato-Asano H, Grossniklaus U, Schulze WX, Robatzek S, Panstruga R ( 2010). PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J Biol Chem 285, 39140-39149. DOI URL PMID
[23]	Li C, Yeh FL, Cheung AY, Duan QH, Kita D, Liu MC, Maman J, Luu EJ, Wu BW, Gates L, Jalal M, Kwong A, Carpenter H, Wu HM ( 2015). Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. eLife 4, e06587. DOI URL
[24]	Li HJ, Yang WC ( 2016). RLKs orchestrate the signaling in plant male-female interaction. Sci China Life Sci 59, 867-877. DOI URL PMID
[25]	Li HJ, Yang WC ( 2018). Ligands switch model for pollen- tube integrity and burst. Trends Plant Sci 23, 369-372. URL PMID
[26]	Li L, Li M, Yu LP, Zhou ZY, Liang XX, Liu ZX, Cai GH, Gao LY, Zhang XJ, Wang YC, Chen S, Zhou JM ( 2014). The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15, 329-338. DOI URL PMID
[27]	Liu LF, Shangguan KK, Zhang BC, Liu XL, Yan MX, Zhang LJ, Shi YY, Zhang M, Qian Q, Li JY, Zhou YH ( 2013). Brittle Culm1, a COBRA-like protein, functions in cellulose assembly through binding cellulose microfibrils. PLoS Genet 9, e1003704. DOI URL PMID
[28]	Liu XL, Castro C, Wang YB, Noble J, Ponvert N, Bundy M, Hoel C, Shpak E, Palanivelu R ( 2016). The role of LORELEI in pollen tube reception at the interface of the synergid cell and pollen tube requires the modified eight- cysteine motif and the receptor-like kinase FERONIA. Plant Cell 28, 1035-1052. URL PMID
[29]	Mangano S, Juárez SPD, Estevez JM ( 2016). ROS regulation of polar growth in plant cells. Plant Physiol 171, 1593-1605. DOI URL PMID
[30]	Mecchia MA, Santos-Fernandez G, Duss NN, Somoza SC, Boisson-Dernier A, Gagliardini V, Martínez-Ber- nardini A, Fabrice TN, Ringli C, Muschietti JP, Gros- sniklaus U ( 2017). RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358, 1600-1603. DOI URL PMID
[31]	Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S ( 2007). Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci USA 104, 20996-21001. DOI URL PMID
[32]	Shen QJ, Bourdais G, Pan HR, Robatzek S, Tang DZ ( 2017). Arabidopsis glycosylphosphatidylinositol-anchored protein LLG1 associates with and modulates FLS2 to regulate innate immunity. Proc Natl Acad Sci USA 114, 5749-5754. URL PMID
[33]	Shi H, Shen QJ, Qi YP, Yan HJ, Nie HZ, Chen YF, Zhao T, Katagiri F, Tang DZ ( 2013). BR-SIGNALING KINASE 1 physically associates with FLAGELLIN SENSING 2 and regulates plant innate immunity in Arabidopsis. Plant Cell 25, 1143-1157. DOI URL PMID
[34]	Sun YD, Li L, Macho AP, Han ZF, Hu ZH, Zipfel C, Zhou JM, Chai JJ ( 2013). Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342, 624-628. DOI URL PMID
[35]	Swanson S, Gilroy S ( 2010). ROS in plant development. Physiol Plant 138, 384-392. DOI URL PMID
[36]	Xiao Y, Stegmann M, Han ZF, DeFalco TA, Parys K, Xu L, Belkhadir Y, Zipfel C, Chai JJ ( 2019). Mechanisms of RALF peptide perception by a heterotypic receptor complex. Nature 572, 270-274. DOI URL PMID
[37]	Xu GY, Chen WJ, Song LM, Chen QS, Zhang H, Liao HD, Zhao GQ, Lin FC, Zhou HN, Yu F ( 2019). FERONIA phosphorylates E3 ubiquitin ligase ATL6 to modulate the stability of 14-3-3 proteins in response to the carbon/nitrogen ratio. J Exp Bot 70, 6375-6388. DOI URL PMID
[38]	Yang T, Wang L, Li CY, Liu Y, Zhu SR, Qi YY, Liu XM, Lin QL, Luan S, Yu F ( 2015). Receptor protein kinase FERO-NIA controls leaf starch accumulation by interacting with glyceraldehyde-3-phosphate dehydrogenase. Biochem Biophys Res Commun 465, 77-82. DOI URL PMID
[39]	Yang YQ, Qin YX, Xie CG, Zhao FY, Zhao JF, Liu DF, Chen SY, Fuglsang AT, Palmgren MG, Schumaker KS, Deng XW, Guo Y ( 2010). The Arabidopsis chaperone J3 regulates the plasma membrane H⁺-ATPase through interaction with the PKS5 kinase. Plant Cell 22, 1313-1332. DOI URL PMID
[40]	Yeats TH, Sorek H, Wemmer DE, Somerville CR ( 2016). Cellulose deficiency is enhanced on hyper accumulation of sucrose by a H⁺-coupled sucrose symporter. Plant Physiol 171, 110-124. DOI URL PMID
[41]	Yin YL, Qin KZ, Song XW, Zhang QH, Zhou YH, Xia XJ, Yu JQ ( 2018). BZR1 transcription factor regulates heat stress tolerance through FERONIA receptor-like kinase- mediated reactive oxygen species signaling in tomato. Plant Cell Physiol 59, 2239-2254. DOI URL PMID
[42]	Yu F, Qian LC, Nibau C, Duan QH, Kita D, Levasseur K, Li XQ, Lu CQ, Li H, Hou CC, Li LG, Buchanan BB, Chen LB, Cheung AY, Li DP, Luan S ( 2012). FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc Natl Acad Sci USA 109, 14693-14698. DOI URL PMID
[43]	Yu JJ, Li Y, Qin Z, Guo SY, Li YF, Miao YC, Song CP, Chen SX, Dai SJ ( 2020). Plant chloroplast stress response: insights from thiol redox proteomics. Antioxid Redox Signal 33, 35-57. DOI URL PMID
[44]	Yu SC, Guo ZW, Johnson C, Gu GF, Wu QY ( 2013). Recent progress in synthetic and biological studies of GPI anchors and GPI-anchored proteins. Curr Opin Chem Biol 17, 1006-1013. DOI URL PMID
[45]	Yu YQ, Assmann SM ( 2015). The heterotrimeric G-protein β subunit, AGB1, plays multiple roles in the Arabidopsis salinity response. Plant Cell Environ 38, 2143-2156. DOI URL PMID
[46]	Yu YQ, Chakravorty D, Assmann SM ( 2018). The G protein β-subunit, AGB1, interacts with FERONIA in RALF1- regulated stomatal movement. Plant Physiol 176, 2426-2440. DOI URL PMID
[47]	Zhang WT, Liu J, Zhang YX, Qiu J, Li Y, Zheng BJ, Hu FH, Dai SJ, Huang XH ( 2020). A high-quality genome sequence of alkaligrass provides insights into halophyte stress tolerance. Sci China Life Sci 63, 1269-1282.
[48]	Zhao CZ, Zayed O, Yu ZP, Jiang W, Zhu PP, Hsu CC, Zhang LR, Tao WA, Lozano-Durán R, Zhu JK ( 2018). Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc Natl Acad Sci USA 115, 13123-13128. DOI URL PMID
[49]	Zhong S, Qu LJ ( 2019). Peptide/receptor-like kinase-mediated signaling involved in male-female interactions. Curr Opin Plant Biol 51, 7-14. DOI URL PMID
[50]	Zurzolo C, Simons K ( 2016). Glycosylphosphatidylinositol-anchored proteins: membrane organization and transport. Biochim Biophys Acta 1858, 632-639. DOI URL PMID