Please wait a minute...
Journal of Integrative Agriculture  2024, Vol. 23 Issue (10): 3487-3505    DOI: 10.1016/j.jia.2024.03.036
Section 3: Cotton molecular design breeding Advanced Online Publication | Current Issue | Archive | Adv Search |
Pectin methylesterase inhibitors GhPMEI53 and AtPMEI19 improve seed germination by modulating cell wall plasticity in cotton and Arabidopsis
Yayue Pei1*, Yakong Wang1*, Zhenzhen Wei1*, Ji Liu2, Yonghui Li3, Shuya Ma3, Ye Wang3, Fuguang Li1, 2#, Jun Peng2, 3#, Zhi Wang1, 2, 3#
1 Zhengzhou Research Base, State Key Laboratory of Cotton Bio-breeding and Integrated Utilization, Zhengzhou University, Zhengzhou 450001, China
2 National Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya 572024, China
3 National Key Laboratory of Cotton Bio-breeding and Integrated Utilization/Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  
果胶甲酯酶(PME)和果胶甲酯酶抑制子(PMEI)通过拮抗方式调控果胶甲酯化程度,在种子萌发中发挥了重要作用,但其中的具体调控机制尚不明晰。我们的研究表明,棉花GhPMEI53的过表达导致PME活性降低,果胶甲酯化程度增加,进而使种子细胞壁软化,最终促进了种子的萌发。GhPMEI53在拟南芥中的同源基因AtPMEI19在种子萌发过程中具有相似的作用,这说明PMEI在种子萌发中的功能和调控机制具有一定的保守性。进一步研究表明GhPMEI53和AtPMEI19促使细胞壁变软,降低其机械强度,从而直接促进胚根突破和种子萌发。通过转录组测序发现,转基因材料中ABA和GA的信号通路发生了显著变化,表明GhPMEI53和AtPMEI19介导的果胶甲酯化过程影响了种子萌发中的激素信号转导。综上所述,GhPMEI53及其同源基因AtPMEI19不仅通过调控果胶甲酯化程度改变细胞壁的力学特性影响胚根突破胚乳和种皮的过程,还通过调控激素信号通路(如ABA, GA)影响种子萌发。这些结果丰富了我们对果胶甲酯化在植物细胞形态动力学和激素信号转导中的认识,也有助于对植物PME/PMEI超基因家族作用机制的全面了解。


Abstract  
The germination process of seeds is influenced by the interplay between two opposing factors, pectin methylesterase (PME) and pectin methylesterase inhibitor (PMEI), which collectively regulate patterns of pectin methylesterification.  Despite the recognized importance of pectin methylesterification in seed germination, the specific mechanisms that govern this process remain unclear.  In this study, we demonstrated that the overexpression of GhPMEI53 is associated with a decrease in PME activity and an increase in pectin methylesterification.  This leads to seed cell wall softening, which positively regulates cotton seed germination.  AtPMEI19, the homologue in Arabidopsis thaliana, plays a similar role in seed germination to GhPMEI53, indicating a conserved function and mechanism of PMEI in seed germination regulation.  Further studies revealed that GhPMEI53 and AtPMEI19 directly contribute to promoting radicle protrusion and seed germination by inducing cell wall softening and reducing mechanical strength.  Additionally, the pathways of abscicic acid (ABA) and gibberellin (GA) in the transgenic materials showed significant changes, suggesting that GhPMEI53/AtPMEI19-mediated pectin methylesterification serves as a regulatory signal for the related phytohormones involved in seed germination.  In summary, GhPMEI53 and its homologs alter the mechanical properties of cell walls, which influence the mechanical resistance of the endosperm or testa.  Moreover, they impact cellular phytohormone pathways (e.g., ABA and GA) to regulate seed germination.  These findings enhance our understanding of pectin methylesterification in cellular morphological dynamics and signaling transduction, and contribute to a more comprehensive understanding of the PME/PMEI gene superfamily in plants.


Keywords:  seed germination        cell wall        pectin demethylesterification        PMEI        ABA  
Received: 16 October 2023   Accepted: 01 February 2024
Fund: 
This study was funded by the National Natural Science Foundation of China (32072022), the Nanfan Special Project, CAAS (YBXM07), and the Hainan Yazhou Bay Seed Laboratory, China (B23CJ0208). 
About author:  #Correspondence Zhi Wang, E-mail: wangzhi01@caas.cn; Jun Peng, E-mail: jun_peng@126.com; Fuguang Li, E-mail: aylifug@caas.cn * These authors contributed equally to this study.

Cite this article: 

Yayue Pei, Yakong Wang, Zhenzhen Wei, Ji Liu, Yonghui Li, Shuya Ma, Ye Wang, Fuguang Li, Jun Peng, Zhi Wang. 2024. Pectin methylesterase inhibitors GhPMEI53 and AtPMEI19 improve seed germination by modulating cell wall plasticity in cotton and Arabidopsis. Journal of Integrative Agriculture, 23(10): 3487-3505.

Ali F, Qanmber G, Li F, Wang Z. 2022. Updated role of ABA in seed maturation, dormancy, and germination. Journal of Advanced Research35, 199–214.

Ali F, Qanmber G, Wei Z, Yu D, Li Y H, Gan L, Li F, Wang Z. 2020. Genome-wide characterization and expression analysis of geranylgeranyl diphosphate synthase genes in cotton (Gossypium spp.) in plant development and abiotic stresses. BMC Genomics21, 561.

Altschul S F, Gish W, Miller W, Myers E W, Lipman D J. 1990. Basic local alignment search tool. Journal of Molecular Biology215, 403–410.

An S H, Sohn K H, Choi H W, Hwang I S, Lee S C, Hwang B K. 2008. Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta228, 61–78.

Bewley J D. 1997. Seed germination and dormancy. Plant Cell9, 1055–1066.

Boisson-Dernier A, Franck C M, Lituiev D S, Grossniklaus U. 2015. Receptor-like cytoplasmic kinase MARIS functions downstream of CrRLK1L-dependent signaling during tip growth. Proceedings of the National Academy of Sciences of the United States of America112, 12211–12216.

Chandra S, Yadav R R, Poonia S, Pal Y, Talukdar A. 2017. Seed coat permeability studies in wild and cultivated species of soybean. Science Advances6, 2358–2363.

Chen F, Bradford K J. 2000. Expression of an expansin is associated with endosperm weakening during tomato seed germination. Plant Physiology124, 1265–1274.

Chen F, Nonogaki H, Bradford K J. 2002. A gibberellin-regulated xyloglucan endotransglycosylase gene is expressed in the endosperm cap during tomato seed germination. Journal of Experimental Botany53, 215–223.

Chen J, Yu F, Liu Y, Du C Q, Li X S, Zhu S R, Wang X C, Lan W Z, Rodriguez P L, Liu X M, Li D P, Chen L B, Luan S. 2016. FERONIA interacts with ABI2-type phosphatases to facilitate signaling cross-talk between abscisic acid and RALF peptide in ArabidopsisProceedings of the National Academy of Sciences of the United States of America113, E5519–E5527.

Coculo D, Lionetti V. 2022. The plant invertase/pectin methylesterase inhibitor superfamily. Frontiers in Plant Science13, 863892.

Cosgrove D J. 2005. Growth of the plant cell wall. Nature Reviews Molecular Cell Biolog6, 850–861.

Donohue K, de Casas R, Burghardt L, Kovach K, Willis C G. 2010. Germination, postgermination adaptation, and species ecological ranges. Annual Review of EcologyEvolutionand Systematics41, 293–319.

Duan Q, Kita D, Li C, Cheung A Y, Wu H M. 2010. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proceedings of the National Academy of Sciences of the United States of America107, 17821–17826.

Fu F F, Peng Y S, Wang G B, Yousry A, El-Kassaby, Cao F L. 2021. Integrative analysis of the metabolome and transcriptome reveals seed germination mechanism in Punica granatum L. Journal of Integrative Agriculture20, 132–146.

Francoz E, Ranocha P, Le Ru A, Martinez Y, Fourquaux I, Jauneau A, Dunand C, Burlat V. 2019. Pectin demethylesterification generates platforms that anchor peroxidases to remodel plant cell wall domains. Developmental Cell48, 261–276.

Ge X Y, Zhang C J, Wang Q H, Yang Z R, Wang Y, Zhang X Y, Wu Z X, Hou Y X, Wu J H, Li F G. 2015. iTRAQ protein profile differential analysis between somatic globular and cotyledonary embryos reveals stress, hormone, and respiration involved in increasing plant let regeneration of Gossypium hirsutum L. Journal of Proteome Research14, 268–278.

Graeber K, Linkies A, Muller K, Wunschova A, Rott A, Leubner-Metzger G. 2010. Cross-species approaches to seed dormancy and germination: Conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes. Plant Molecular Biology73, 67–87.

Guénin S, Hardouin J, Paynel F, Müller K, Mongelard G, Driouich A, Lerouge P, Kermode A R, Lehner A, Mollet J C, Pelloux J, Gutierrez L, Mareck A. 2017. AtPME3, a ubiquitous cell wall pectin methylesterase of Arabidopsis thaliana, alters the metabolism of cruciferin seed storage proteins during post-germinative growth of seedlings. Journal of Experimental Botany68, 1083–1095.

Guénin S, Mareck A, Rayon C, Lamour R, Assoumou Ndong Y, Domon J M, Senechal F, Fournet F, Jamet E, Canut H, Percoco G, Mouille G, Rolland A, Rusterucci C, Guerineau F, Van Wuytswinkel O, Gillet F, Driouich A, Lerouge P, Gutierrez L, et al. 2011. Identification of pectin methylesterase 3 as a basic pectin methylesterase isoform involved in adventitious rooting in Arabidopsis thalianaNew Phytologist192, 114–126.

Guzha A, McGee R, Scholz P, Hartken D, Lüdke D, Bauer K, Wenig M, Zienkiewicz K, Herrfurth C, Feussner I, Vlot A C, Wiermer M, Haughn G, Ischebeck T. 2022. Cell wall-localized BETA-XYLOSIDASE4 contributes to immunity of Arabidopsis against Botrytis cinereaPlant Physiology189, 1794–1813.

He W, Zhao H M, Yang X W, Zhang R, Wang J J. 2019. Patent analysis provides insights into the history of cotton molecular breeding worldwide over the last 50 years. Journal of Integrative Agriculture18, 539–552.

Herburger K, Schoenaers S, Vissenberg K, Mravec J. 2022. Shank-localized cell wall growth contributes to Arabidopsis root hair elongation. Nature Plants8, 1222–1232.

Huang J, Yang L, Yang L, Wu X, Cui X, Zhang L, Hui J, Zhao Y, Yang H, Liu S, Xu Q, Pang M, Guo X, Cao Y, Chen Y, Ren X, Lv J, Yu J, Ding J, Xu G, et al. 2023. Stigma receptors control intraspecies and interspecies barriers in Brassicaceae. Nature614, 303–308.

Hughes D W, Wang H Y C, Galau G A. 1993. Cotton (Gossypium hirsutum) MatP6 and MatP7 oleosin genes. Plant Physiology101, 697–698.

Kohorn B D, Kohorn S L, Saba N J, Martinez V M. 2014. Requirement for pectin methyl esterase and preference for fragmented over native pectins for wall-associated kinase-activated, EDS1/PAD4-dependent stress response in ArabidopsisJournal of Biological Chemistry289, 18978–18986.

Leubner-Metzger G, Frundt C, Vogeli-Lange R, Meins Jr F. 1995. Class I [beta]-1,3-glucanases in the endosperm of tobacco during germination. Plant Physiology109, 751–759.

Levesque-Tremblay G, Müller K, Mansfield S D, Haughn G W. 2015. HIGHLY METHYL ESTERIFIED SEEDS is a pectin methyl esterase involved in embryo development. Plant Physiology167, 725–737.

Li E, Wang G, Zhang Y L, Kong Z, Li S. 2020. FERONIA mediates root nutating growth. The Plant Journal104, 1105–1116.

Lin W, Tang W, Pan X, Huang A, Gao X, Anderson C T, Yang Z. 2022. Arabidopsis pavement cell morphogenesis requires FERONIA binding to pectin for activation of ROP GTPase signaling. Current Biology32, 497–507.

Linkies A, Muller K, Morris K, Tureckova V, Wenk M, Cadman C S C, Corbineau F, Strnad M, Lynn J R, Finch-Savage W E, Leubner-Metzger G. 2009. Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: A comparative approach using lepidium sativum and Arabidopsis thalianaPlant Cell21, 3803–3822.

Müller K, Levesque-Tremblay G, Bartels S, Weitbrecht K, Wormit A, Usadel B, Haughn G, Kermode A R. 2013. Demethylesterification of cell wall pectins in Arabidopsis plays a role in seed germination. Plant Physiology161, 305–316.

Müller K, Tintelnot S, Leubner-Metzger G. 2006. Endosperm-limited Brassicaceae seed germination: Abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thalianaPlant and Cell Physiology47, 864–877.

Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E. 2005. Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: Epigenetic and genetic regulation of transcription in seed. The Plant Journal41, 697–709.

Nonogaki H, Gee O H, Bradford K J. 2000. A germination-specific endo-beta-mannanase gene is expressed in the micropylar endosperm cap of tomato seeds. Plant Physiology123, 1235–1245.

Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E. 2006. CYP707A1 and CYP707A2, which encode abscisic acid 8´-hydroxylases, are indispensable for proper control of seed dormancy and germination in ArabidopsisPlant Physiology141, 97–107.

Pahlavani M, Miri A, Kazemi G. 2009. Response of oil and protein content to seed size in cotton (Gossypium hirsutum L. cv. Sahel). Plant Breeding and Seed Science59, 53–64.

Peaucelle A, Braybrook S, Hofte H. 2012. Cell wall mechanics and growth control in plants: the role of pectins revisited. Frontiers in Plant Science3, 121.

Pinto L V A, Da Silva E A A, Davide A C, De Jesus V A M, Toorop P E, Hilhorst H W M. 2007. Mechanism and control of Solanum lycocarpum seed germination. Annals of Botany100, 1175–1187.

Quettier A L, Bertrand C, Habricot Y, Miginiac E, Agnes C, Jeannette E, Maldiney R. 2006. The phs1-3 mutation in a putative dual-specificity protein tyrosine phosphatase gene provokes hypersensitive responses to abscisic acid in Arabidopsis thalianaThe Plant Journal47, 711–719.

Ren C, Kermode A R. 2000. An increase in pectin methyl esterase activity accompanies dormancy breakage and germination of yellow cedar seeds. Plant Physiology124, 231–242.

Saez-Aguayo S, Ralet M C, Berger A, Botran L, Ropartz D, Marion-Poll A, North H M. 2013. PECTIN METHYLESTERASE INHIBITOR6 promotes Arabidopsis mucilage release by limiting methylesterification of homogalacturonan in seed coat epidermal cells. Plant Cell25, 308–323.

Sampedro J, Gianzo C, Iglesias N, Guitián E, Revilla G, Zarra I. 2012. AtBGAL10 is the main xyloglucan β-Galactosidase in Arabidopsis, and its absence results in unusual xyloglucan subunits and growth defects. Plant Physiology158, 1146–1157.

Sánchez R A, De Miguel L. 1997. Phytochrome promotion of mannan-degrading enzyme activities in the micropylar endosperm of Datura ferox seeds requires the presence of the embryo and gibberellin synthesis. Seed Science Research7, 27–34.

Senechal F, Wattier C, Rusterucci C, Pelloux J. 2014. Homogalacturonan-modifying enzymes: Structure, expression, and roles in plants. Journal of Experimental Botany65, 5125–5160.

Shi D C, Ren A Y, Tang X F, Qi G, Xu Z C, Chai G H, Hu R B, Zhou G K, Kong Y Z. 2018. Myb52 negatively regulates pectin demethylesterification in seed coat mucilage. Plant Physiology176, 2737–2749.

Silva-Sanzana C, Celiz-Balboa J, Garzo E, Marcus S E, Blanco-Herrera F. 2019. Pectin methyesterases modulate plant homogalacturonan status in defenses against the Aphid Myzus persicaeThe Plant Cell31, 1913–1929.

Sun J, Yuan C, Wang M, Ding A, Chai G, Sun Y, Zhao G, Yang D, Kong Y. 2021. MUD1, a RING-v E3 ubiquitin ligase, has an important role in the regulation of pectin methylesterification in Arabidopsis seed coat mucilage. Plant Physiology and Biochemistry168, 230–238.

Turbant A, Fournet F, Lequart M, Zabijak L, Pageau K, Bouton S, Van Wuytswinkel O. 2016. PME58 plays a role in pectin distribution during seed coat mucilage extrusion through homogalacturonan modification. Journal of Experimental Botany67, 2177–2190.

Verma P, Kaur H, Petla B P, Rao V, Saxena S C, Majee M. 2013. PROTEIN L-ISOASPARTYL METHYLTRANSFERASE2 is differentially expressed in chickpea and enhances seed vigor and longevity by reducing abnormal isoaspartyl accumulation predominantly in seed nuclear proteins. Plant Physiology161, 1141–1157.

Wang H H, Qiu Y, Yu Q, Zhang Q, Li X, Wang J, Li X, Zhang Y, Yang Y. 2020. Close arrangement of CARK3 and PMEIL affects ABA-mediated pollen sterility in Arabidopsis thalianaPlant Cell Environment43, 2699–2711.

Wang M H, Liu M X, Li D K, Wu J, Li X F, Yang Y. 2010. Overexpression of FAD2 promotes seed germination and hypocotyl elongation in Brassica napusPlant CellTissue and Organ Culture102, 205–211.

Wang Y, Yan H, Wang Q, Zhang R, Xia K, Liu Y. 2020. Regulation of the phytotoxic response of Arabidopsis thaliana to the Fusarium mycotoxin deoxynivalenol. Journal of Integrative Agriculture19, 759–767.

Wang Z, Cao H, Sun Y, Li X, Chen F, Carles A, Li Y, Ding M, Zhang C, Deng X, Soppe W J, Liu Y X. 2013. Arabidopsis paired amphipathic helix proteins SNL1 and SNL2 redundantly regulate primary seed dormancy via abscisic acid-ethylene antagonism mediated by histone deacetylation. Plant Cell25, 149–166.

Wei Z, Li Y, Ali F, Wang Y, Liu J, Yang Z, Wang Z, Xing Y, Li F. 2022. Transcriptomic analysis reveals the key role of histone deacetylation via mediating different phytohormone signalings in fiber initiation of cotton. Cell and Bioscience12, 107.

Weitbrecht K, Muller K, Leubner-Metzger G. 2011. First off the mark: Early seed germination. Journal of Experimental Botany62, 3289–3309.

Wolf S, Mravec J, Greiner S, Mouille G, Hofte H. 2012. Plant cell wall homeostasis is mediated by brassinosteroid feedback signaling. Current Biology22, 1732–1737.

Wormit A, Usadel B. 2018. The multifaceted role of pectin methylesterase inhibitors (PMEIs). International Journal of Molecular Sciences19, 2878.

Wu J, Mao X, Cai T, Luo J, Wei L. 2006. KOBAS server: A web-based platform for automated annotation and pathway identification. Nucleic Acids Research34, W720–W724.

Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li C Y, Wei L. 2011. KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Research39, W316–W322.

Yamaguchi S, Kamiya Y, Nambara E. 2007. Regulation of ABA and GA Levels during seed development and germination in ArabidopsisAnnual Plant Reviews27, 224–247.

Yue Z L, Liu N, Deng Z P, Zhang Y, Wu Z M, Zhao J L, Sun Y, Wang Z Y, Zhang S W. 2022. The receptor kinase OsWAK11 monitors cell wall pectin changes to fine-tune brassinosteroid signaling and regulate cell elongation in rice. Current Biology32, 2454–2466.

Zang X, Pei W F, Wu M, Geng Y, Wang N, Liu G, Ma J, Li D, Cui Y, Li X, Zhang J, Yu J J. 2018. Genome-scale analysis of the WRI-like family in Gossypium and functional characterization of GhWRI1a controlling triacylglycerol content. Friontiers in Plant Science9, 1516.

Zaqout S, Becker L L, Kaindl A M. 2020. Immunofluorescence staining of paraffin sections step by step. Front Neuroanat14, 582218.

Zhang J, Liu H, Sun J, Li B, Zhu Q, Chen S, Zhang H. 2012. Arabidopsis fatty acid desaturase FAD2 is required for salt tolerance during seed germination and early seedling growth. PLoS ONE7, e30355.

Zhang X, Guo H, Xiao C, Yan Z, Ning N, Chen G, Zhang J, Hu H. 2023. PECTIN METHYLESTERASE INHIBITOR18 functions in stomatal dynamics and stomatal dimension. Plant Physiology192, 1603–1620.

Zhang X, Henriques R, Lin S S, Niu Q W, Chua N H. 2006. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature Protocols1, 641–646.

Zhang Z L, Ogawa M, Fleet C M, Zentella R, Hu J, Heo J O, Lim J, Kamiya Y, Yamaguchi S, Sun T P. 2011. Scarecrow-like 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in ArabidopsisProceedings of the National Academy of Sciences of the United States of America108, 2160–2165.

[1] ZHANG Yu-zheng, XU Chen, LU Wen-li, WANG Xiao-zhe, WANG Ning, MENG Xiang-guang, FANG Yu-hui, TAN Qiu-ping, CHEN Xiu-de, FU Xi-ling, LI Ling.

PpMAPK6 regulates peach bud endodormancy release through interactions with PpDAM6 [J]. >Journal of Integrative Agriculture, 2023, 22(1): 139-148.

No Suggested Reading articles found!