PIP/PIPL：一类调控植物逆境响应和发育的植物内源性多肽

doi:10.13560/j.cnki.biotech.bull.1985.2022-0816

摘要/Abstract

摘要：

植物内源性多肽由前体蛋白剪切而成，由天然氨基酸以不同组成和排列方式构成。多肽分泌至细胞外后，被其受体识别，从而调控植物生长发育和逆境响应。PIP（PAMP-induced secreted peptide）/PIP-Like（PIPL）是包含SGPS和GxGH基序的植物内源性多肽，可被受体激酶RLK7（receptor-like kinase 7）识别，在植物抵抗病原菌、病毒和盐害等逆境及调控生长发育过程中扮演重要角色。本文重点阐述了PIP/PIPL家族多肽在植物抵抗逆境胁迫和调控生长发育过程中的信号转导通路，并讨论了该领域尚待解决的一些科学问题和可能的应用方向，以期为PIP/PIPL的深入研究提供参考。

关键词: PIP/PIPL, RLK7, 信号转导, 逆境, 发育

Abstract:

Plant endogenous polypeptides are composed of natural amino acids in different composition and arrangement from the precursor proteins cut into mature polypeptides, which play biological function in development and stress response after secreted outside the cells and recognized by their receptors. The plant endogenous polypeptide family PIP（PAMP induced secret peptide）/PIP-Like（PIPL）contains SGPS and GxGH motifs recognized by receptor like kinase 7（RLK7）, and plays important roles in pathogen resistance, virus resistance, salt resistance and development. Here, we review the signal transduction pathways of PIP/PIPL family polypeptides in the process of resistance to stress and development, discuss important unsolved scientific issues, and prospect possible applications, aiming to provide the references on further researches on PIP/PIPL.

Key words: PIP/PIPL, RLK7, signal transduction, stress, development

崔俊美, 魏家萍, 董小云, 王莹, 郑国强, 刘自刚. PIP/PIPL：一类调控植物逆境响应和发育的植物内源性多肽[J]. 生物技术通报, 2023, 39(3): 35-42.

CUI Jun-mei, WEI Jia-ping, DONG Xiao-yun, WANG Ying, ZHENG Guo-qiang, LIU Zi-gang. PIP/PIPL: A Kind of Endogenous Plant Peptide Regulating Plant Stress Response and Development[J]. Biotechnology Bulletin, 2023, 39(3): 35-42.

图/表 5

图1 AtPIP/PIPL家族蛋白质序列比对及保守基序分析 A：基于AtPIP/PIPL前体蛋白全长序列的蛋白质比对，保守基序用红色标注。 B：AtPIP/PIPL的保守序列特征

Fig. 1 Sequence alignment and conserved motif of AtPIP/PIPL family proteins A: Alignment based on full-length sequence of AtPIP/PIPL precursor proteins. The conserved motifs were marked in red. B: Conserved sequence features of AtPIP/PIPL

图2 RLK7蛋白结构及LRRs序列信息 A：RLK7蛋白结构信息；B：RLK7的LRRs基序信息

Fig. 2 Protein structure and LRRs sequence information of RLK7 A: Structural information of RLK7 protein. B: LRRs motif information of RLK7

图3 RLK7受体复合物

Fig. 3 RLK7 receptor complex

图4 LRR XI亚家族成员及其他几个RLKs的激酶域序列比对分析 *：磷酸化或激酶活性位点

Fig. 4 Alignment analysis of kinase domain sequences of LRR XI subfamily members and other RLKs * indicates phosphorylation or kinase active sites

图5 PIP/PIPL信号转导示意图

Fig. 5 Schematic diagram of PIP/PIPL signal transduction

参考文献 47

[1]	Matsubayashi Y, Sakagami Y. Peptide hormones in plants[J]. Annu Rev Plant Biol, 2006, 57: 649-674. pmid: 16669777
[2]	Matsubayashi Y. Posttranslationally modified small-peptide signals in plants[J]. Annu Rev Plant Biol, 2014, 65: 385-413. doi: 10.1146/annurev-arplant-050312-120122 pmid: 24779997
[3]	Lease KA, Walker JC. Bioinformatic identification of plant peptides[J]. Methods Mol Biol, 2010, 615: 375-383. doi: 10.1007/978-1-60761-535-4_26 pmid: 20013221
[4]	Lease KA, Walker JC. The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics[J]. Plant Physiol, 2006, 142(3): 831-838. doi: 10.1104/pp.106.086041 URL
[5]	Takahashi F, Suzuki T, Osakabe Y, et al. A small peptide modulates stomatal control via abscisic acid in long-distance signalling[J]. Nature, 2018, 556(7700): 235-238. doi: 10.1038/s41586-018-0009-2
[6]	Takahashi F, Hanada K, Kondo T, et al. Hormone-like peptides and small coding genes in plant stress signaling and development[J]. Curr Opin Plant Biol, 2019, 51: 88-95. doi: S1369-5266(19)30028-7 pmid: 31265991
[7]	Huffaker A, Pearce G, Ryan CA. An endogenous peptide signal in Arabidopsis activates components of the innate immune response[J]. PNAS, 2006, 103(26): 10098-10103. doi: 10.1073/pnas.0603727103 pmid: 16785434
[8]	Stegmann M, Monaghan J, Smakowska-Luzan E, et al. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling[J]. Science, 2017, 355(6322): 287-289. doi: 10.1126/science.aal2541 pmid: 28104890
[9]	Zhou HP, Xiao F, Zheng Y, et al. Pamp-induced secreted peptide 3 modulates salt tolerance through receptor-like kinase 7 in plants[J]. Plant Cell, 2022, 34(2): 927-944. doi: 10.1093/plcell/koab292 URL
[10]	Najafi J, Brembu T, Vie AK, et al. Pamp-induced secreted peptide 3(pip3)modulates immunity in Arabidopsis thaliana[J]. J Exp Bot, 2020, 71(3):850-864. doi: 10.1093/jxb/erz482 pmid: 31665431
[11]	Hussain S, Wang W, Ahmed S, et al. PIP2, an auxin induced plant peptide hormone regulates root and hypocotyl elongation in Arabidopsis[J]. Front Plant Sci, 2021, 12: 646736. doi: 10.3389/fpls.2021.646736 URL
[12]	Hou SG, Wang X, Chen DH, et al. The secreted peptide PIP1 amplifies immunity through receptor-like kinase 7[J]. PLoS Pathog, 2014, 10(9): e1004331. doi: 10.1371/journal.ppat.1004331 URL
[13]	Vie AK, Najafi J, Liu B, et al. The IDA/IDA-LIKE and PIP/PIP-LIKE gene families in Arabidopsis: phylogenetic relationship, expression patterns, and transcriptional effect of the PIPL3 peptide[J]. J Exp Bot, 2015, 66(17): 5351-5365. doi: 10.1093/jxb/erv285 URL
[14]	Combest MM, Moroz N, Tanaka K, et al. StPIP1, a PAMP-induced peptide in potato, elicits plant defenses and is associated with disease symptom severity in a compatible interaction with Potato virus Y[J]. J Exp Bot, 2021, 72(12): 4472-4488. doi: 10.1093/jxb/erab078 pmid: 33681961
[15]	Ito Y, Nakanomyo I, Motose H, et al. Dodeca-CLE peptides as suppressors of plant stem cell differentiation[J]. Science, 2006, 313(5788): 842-845. doi: 10.1126/science.1128436 pmid: 16902140
[16]	Meng L, Buchanan BB, Feldman LJ, et al. CLE-like(CLEL)peptides control the pattern of root growth and lateral root development in Arabidopsis[J]. Proc Natl Acad Sci USA, 2012, 109(5): 1760-1765. doi: 10.1073/pnas.1119864109 URL
[17]	Aalen RB, Wildhagen M, Stø IM, et al. IDA: a peptide ligand regulating cell separation processes in Arabidopsis[J]. J Exp Bot, 2013, 64(17): 5253-5261. doi: 10.1093/jxb/ert338 URL
[18]	Zipfel C. Plant pattern-recognition receptors[J]. Trends Immunol, 2014, 35(7): 345-351. doi: 10.1016/j.it.2014.05.004 pmid: 24946686
[19]	Belkhadir Y, Yang L, Hetzel J, et al. The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors[J]. Trends Biochem Sci, 2014, 39(10): 447-456. doi: 10.1016/j.tibs.2014.06.006 pmid: 25089011
[20]	Jones JDG, Dangl JL. The plant immune system[J]. Nature, 2006, 444(7117): 323-329. doi: 10.1038/nature05286
[21]	Gómez-Gómez L, Boller T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis[J]. Mol Cell, 2000, 5(6): 1003-1011. doi: 10.1016/s1097-2765(00)80265-8 pmid: 10911994
[22]	Böhm H, et al. A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immunity in Arabidopsis[J]. PLoS Pathog, 2014, 10(11): e1004491. doi: 10.1371/journal.ppat.1004491 URL
[23]	Sakamoto T, Deguchi M, Brustolini OJB, et al. The tomato RLK superfamily: phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense[J]. BMC Plant Biol, 2012, 12: 229. doi: 10.1186/1471-2229-12-229 pmid: 23198823
[24]	Dunning FM, Sun WX, Jansen KL, et al. Identification and mutational analysis of Arabidopsis FLS2 leucine-rich repeat domain residues that contribute to flagellin perception[J]. Plant Cell, 2007, 19(10): 3297-3313. doi: 10.1105/tpc.106.048801 pmid: 17933906
[25]	Tang J, Han ZF, Sun YD, et al. Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1[J]. Cell Res, 2015, 25(1): 110-120. doi: 10.1038/cr.2014.161 pmid: 25475059
[26]	Zhang XX, Liu WJ, Nagae TT, et al. Structural basis for receptor recognition of pollen tube attraction peptides[J]. Nat Commun, 2017, 8(1): 1331. doi: 10.1038/s41467-017-01323-8 pmid: 29109411
[27]	Hallgren J, Tsirigos KD, Pedersen MD, et al. DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks[J]. bioRxiv, 2022, DOI:10.1101/2022.04.08.487609. doi: 10.1101/2022.04.08.487609
[28]	Chen TS. Identification and characterization of the LRR repeats in plant LRR-RLKs[J]. BMC Mol Cell Biol, 2021, 22(1): 9. doi: 10.1186/s12860-021-00344-y pmid: 33509084
[29]	Liebrand TWH, van den Burg HA, Joosten MHAJ. Two for all: receptor-associated kinases SOBIR1 and BAK1[J]. Trends Plant Sci, 2014, 19(2): 123-132. doi: 10.1016/j.tplants.2013.10.003 pmid: 24238702
[30]	Roux M, Schwessinger B, Albrecht C, et al. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens[J]. Plant Cell, 2011, 23(6): 2440-2455. doi: 10.1105/tpc.111.084301 URL
[31]	Liang XX, Zhou JM. Receptor-like cytoplasmic kinases: central players in plant receptor kinase-mediated signaling[J]. Annu Rev Plant Biol, 2018, 69: 267-299. doi: 10.1146/annurev-arplant-042817-040540 pmid: 29719165
[32]	Zhang J, Li W, Xiang TT, et al. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector[J]. Cell Host Microbe, 2010, 7(4): 290-301. doi: 10.1016/j.chom.2010.03.007 pmid: 20413097
[33]	Lei JX, Finlayson SA, Salzman RA, et al. BOTRYTIS-INDUCED KINASE1 modulates Arabidopsis resistance to green peach aphids via PHYTOALEXIN DEFICIENT4[J]. Plant Physiol, 2014, 165(4): 1657-1670. doi: 10.1104/pp.114.242206 URL
[34]	Lu DP, Wu SJ, Gao XQ, et al. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity[J]. PNAS, 2010, 107(1): 496-501. doi: 10.1073/pnas.0909705107 pmid: 20018686
[35]	Liu Z, Wu Y, Yang F, et al. BIK1 interacts with PEPRs to mediate ethylene-induced immunity[J]. Proc Natl Acad Sci USA, 2013, 110(15): 6205-6210. doi: 10.1073/pnas.1215543110 pmid: 23431184
[36]	Macho AP, Lozano-Durán R, Zipfel C. Importance of tyrosine phosphorylation in receptor kinase complexes[J]. Trends Plant Sci, 2015, 20(5): 269-272. doi: S1360-1385(15)00050-3 pmid: 25795237
[37]	Macho AP, Schwessinger B, Ntoukakis V, et al. A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation[J]. Science, 2014, 343(6178): 1509-1512. doi: 10.1126/science.1248849 pmid: 24625928
[38]	Perraki A, DeFalco TA, Derbyshire P, et al. Phosphocode-dependent functional dichotomy of a common co-receptor in plant signalling[J]. Nature, 2018, 561(7722): 248-252. doi: 10.1038/s41586-018-0471-x
[39]	Chinchilla D, Zipfel C, Robatzek S, et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence[J]. Nature, 2007, 448(7152): 497-500. doi: 10.1038/nature05999
[40]	Hartmann J, Fischer C, et al. Kinase activity and calmodulin binding are essential for growth signaling by the phytosulfokine receptor PSKR1[J]. Plant J, 2014, 78(2): 192-202. doi: 10.1111/tpj.12460 URL
[41]	Hou SG, Shen HX, Shao HW. PAMP-induced peptide 1 cooperates with salicylic acid to regulate stomatal immunity in Arabidopsis thaliana[J]. Plant Signal Behav, 2019, 14(11): 1666657. doi: 10.1080/15592324.2019.1666657 URL
[42]	Yamaguchi Y, Pearce G, Ryan CA. The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells[J]. Proc Natl Acad Sci USA, 2006, 103(26): 10104-10109. pmid: 16785433
[43]	Yamaguchi Y, Huffaker A, et al. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis[J]. Plant Cell, 2010, 22(2): 508-522. doi: 10.1105/tpc.109.068874 URL
[44]	Park CH, Bi Y, et al. Deconvoluting signals downstream of growth and immune receptor kinases by phosphocodes of the BSU1 family phosphatases[J]. Nat Plants, 2022, 8(6): 646-655. doi: 10.1038/s41477-022-01167-1 pmid: 35697730
[45]	Toyokura K, Goh T, Shinohara H, et al. Lateral inhibition by a peptide hormone-receptor cascade during Arabidopsis lateral root founder cell formation[J]. Dev Cell, 2019, 48(1): 64-75.e5. doi: S1534-5807(18)30987-0 pmid: 30581155
[46]	Okushima Y, Fukaki H, Onoda M, et al. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis[J]. Plant Cell, 2007, 19(1): 118-130. doi: 10.1105/tpc.106.047761 pmid: 17259263
[47]	Jing YP, Zheng XJ, et al. Danger-associated peptides interact with PIN-dependent local auxin distribution to inhibit root growth in Arabidopsis[J]. Plant Cell, 2019, 31(8): 1767-1787. doi: 10.1105/tpc.18.00757 URL