Chinese Bulletin of Botany ›› 2020, Vol. 55 ›› Issue (5): 541-550.DOI: 10.11983/CBB20058
• INVITED REVIEW • Previous Articles Next Articles
Sijia Li1, Yongxue Zhang1, Mingsheng Jia2, Ying Li1, Shaojun Dai2,*()
Received:
2020-04-05
Accepted:
2020-05-20
Online:
2020-09-01
Published:
2020-09-03
Contact:
Shaojun Dai
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.
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.
[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 |
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