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Genome-Wide Identification of Malectin/Malectin-Like Domain Containing Protein Family Genes in Rice and Their Expression Regulation Under Various Hormones, Abiotic Stresses, and Heavy Metal Treatments

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Abstract

Malectin/malectin-like domain containing proteins are a novel identified protein subfamily of lectins that regulates various functional bioprocesses in plants. However, little is known about the phylogenetic relationships and functions of this gene family in rice. Here, in this study, a total of 84 malectin/malectin-like domain containing proteins, including 67 malectin/malectin-like receptor-like kinases (MRLKs) and 17 malectin/malectin-like receptor-like proteins (MRLPs), were identified in rice. These MRLK and MRLP proteins can be classified into four subfamilies based on the malectin/malectin-like domain present in their extracellular regions. The OsMRLK and OsMRLP gene family members are localized on all the chromosomes in rice genome with the members within the same subfamily sharing similar exon–intron distribution and motif composition. The multiple members and diverse gene and protein structures demonstrate that the malectin/malectin-like domain protein family underscores a functional diversity and divergence in rice. In addition, the expression levels of the OsMRLK gene family members are greatly varied between the tissues and organs at different developmental stages of rice. Furthermore, the majority of the tested OsMRLKs showed significant upregulation in transcripts under a number of abiotic stresses, hormonal applications, and heavy metals, suggesting the vital roles of the OsMRLK genes in rice development and multi-stress tolerance. The results obtained here provide a well fundament for further clarification of the roles of the malectin/malectin-like domain containing proteins in plants.

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References

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34:W369–W373

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baldoni E, Bagnaresi P, Locatelli F, Mattana M, Genga A (2016) Comparative leaf and root transcriptomic analysis of two rice japonica cultivars reveals major differences in the root early response to osmotic stress. Rice 9:25

    PubMed  PubMed Central  Google Scholar 

  • Beale KM, Johnson MA (2013) Speed dating, rejection, and finding the perfect mate: advice from flowering plants. Curr Opin Plant Biol 16:590–597

    CAS  PubMed  Google Scholar 

  • Bellande K, Bono J-J, Savelli B, Jamet E, Canut H (2017) Plant lectins and lectin receptor-like kinases: how do they sense the outside? Int J Mol Sci 18:1164

    PubMed Central  Google Scholar 

  • Berger F, Hamamura Y, Ingouff M, Higashiyama T (2008) Double fertilization-caught in the act. Trends Plant Sci 13:437–443

    CAS  PubMed  Google Scholar 

  • Boisson-Dernier A, Kessler SA, Grossniklaus U (2011) The walls have ears: the role of plant CrRLK1Ls in sensing and transducing extracellular signals. J Exp Bot 62:1581–1591

    CAS  PubMed  Google Scholar 

  • Boisson-Dernier A, Lituiev DS, Nestorova A, Franck CM, Thirugnanarajah S, Grossniklaus U (2013) ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol 11:e1001719

    PubMed  PubMed Central  Google Scholar 

  • Buti M, Pasquariello M, Ronga D, Milc JA, Pecchioni N, Ho VT, Pucciariello C, Perata P, Francia E (2018) Transcriptome profiling of short-term response to chilling stress in tolerant and sensitive Oryza sativa ssp. Japonica seedlings. Funct Integr Genom 18:627–644

    CAS  Google Scholar 

  • Chen J, Yu F, Liu Y, Du C, Li X, Zhu S, Wang X, Lan W, Rodriguez PL, Liu X (2016) FERONIA interacts with ABI2-type phosphatases to facilitate signaling cross-talk between abscisic acid and RALF peptide in Arabidopsis. Proc Natl Acad Sci USA 113:E5519

    CAS  PubMed  Google Scholar 

  • Damme EJMV, Lannoo N, Peumans WJ (2008) Plant lectins. Adv Bot Res 48:107–209

    Google Scholar 

  • Deslauriers SD, Larsen PB (2010) FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Mol Plant 3:626–640

    CAS  PubMed  Google Scholar 

  • Dresselhaus T (2006) Cell–cell communication during double fertilization. Curr Opin Plant Biol 9:41–47

    CAS  PubMed  Google Scholar 

  • Dresselhaus T, Franklin-Tong N (2013) Male–female crosstalk during pollen germination, tube growth and guidance, and double fertilization. Mol Plant 6:1018–1036

    CAS  PubMed  Google Scholar 

  • Duan Q, Kita D, Johnson EA, Aggarwal M, Gates L, Wu H-M, Cheung AY (2014) Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun 5:3129

    PubMed  Google Scholar 

  • Escobar-Restrepo J-M, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang W-C, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317:656–660

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    PubMed  Google Scholar 

  • Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, Liu M-C, Maman J, Steinhorst L, Schmitz-Thom I (2018) The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr Biol 28(666–675):e665

    Google Scholar 

  • Formentin E, Sudiro C, Perin G, Riccadonna S, Barizza E, Baldoni E, Lavezzo E, Stevanato P, Sacchi GA, Fontana P (2018) Transcriptome and cell physiological analyses in different rice cultivars provide new insights into adaptive and salinity stress responses. Front Plant Sci 9:204

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Galindo-Trigo S, Gray JE, Smith LM (2016) Conserved roles of CrRLK1L receptor-like kinases in cell expansion and reproduction from algae to angiosperms. Front Plant Sci 7:1269

    PubMed  PubMed Central  Google Scholar 

  • Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y (2009a) Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci 106(18):7648–7653

    CAS  PubMed  Google Scholar 

  • Guo H, Ye H, Li L, Yin Y (2009b) A family of receptor-like kinases are regulated by BES1 and involved in plant growth in Arabidopsis thaliana. Plant Signal Behav 4:784–786

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hamamura Y, Nishimaki M, Takeuchi H, Geitmann A, Kurihara D, Higashiyama T (2014) Live imaging of calcium spikes during double fertilization in Arabidopsis. Nat Commun 5:4722

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hématy K, Höfte H (2008) Novel receptor kinases involved in growth regulation. Curr Opin Plant Biol 11:321–328

    PubMed  Google Scholar 

  • Hématy K, Sado P-E, Van Tuinen A, Rochange S, Desnos T, Balzergue S, Pelletier S, Renou J-P, Höfte H (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol 17:922–931

    PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:357–359

    Google Scholar 

  • Hou Y, Guo X, Cyprys P, Zhang Y, Bleckmann A, Cai L, Huang Q, Luo Y, Gu H, Dresselhaus T (2016) Maternal ENODLs are required for pollen tube reception in Arabidopsis. Curr Biol 26:2343–2350

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    PubMed  PubMed Central  Google Scholar 

  • Huang G-Q, Li E, Ge F-R, Li S, Wang Q, Zhang C-Q, 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

    CAS  PubMed  Google Scholar 

  • Huck N, Moore JM, Federer M, Grossniklaus U (2003) The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130:2149–2159

    CAS  PubMed  Google Scholar 

  • Kanaoka MM, Torii KU (2010) FERONIA as an upstream receptor kinase for polar cell growth in plants. Proc Natl Acad Sci 107:17461–17462

    CAS  PubMed  Google Scholar 

  • Kawashima T, Berger F (2011) Green love talks; cell–cell communication during double fertilization in flowering plants. AoB Plants. https://doi.org/10.1093/aobpla/plr015

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazaki T, Senzaki E, Hamamura Y, Higashiyama T (2014) Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 113:120642

    Google Scholar 

  • Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330:968–971

    CAS  PubMed  Google Scholar 

  • Kessler SA, Lindner H, Jones DS, Grossniklaus U (2015) Functional analysis of related CrRLK1L receptor-like kinases in pollen tube reception. EMBO Rep 16:107–115

    CAS  PubMed  Google Scholar 

  • Kong H, Landherr LL, Frohlich MW, Leebens-Mack J, Ma H, DePamphilis CW (2007) Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J 50:873–885

    CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870

    CAS  Google Scholar 

  • Lassig R, Gutermuth T, Bey TD, Konrad KR, Romeis T (2014) Pollen tube NAD (P) H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J 78:94–106

    CAS  PubMed  Google Scholar 

  • Li C, Yeh F-L, Cheung AY, Duan Q, Kita D, Liu M-C, Maman J, Luu EJ, Wu BW, Gates L (2015) Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. Elife 4:e06587

    PubMed Central  Google Scholar 

  • Lindner H, Müller LM, Boisson-Dernier A, Grossniklaus U (2012) CrRLK1L receptor-like kinases: not just another brick in the wall. Curr Opin Plant Biol 15:659–669

    CAS  PubMed  Google Scholar 

  • Loris R (2002) Principles of structures of animal and plant lectins. Biochim Biophys Acta 1572:198–208

    CAS  PubMed  Google Scholar 

  • Mao D, Yu F, Li J, Van de Poel B, Tan D, Li J, Liu Y, Li X, Dong M, Chen L (2015) FERONIA receptor kinase interacts with S-adenosylmethionine synthetase and suppresses S-adenosylmethionine production and ethylene biosynthesis in Arabidopsis. Plant, Cell Environ 38:2566–2574

    CAS  Google Scholar 

  • Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, Fukuda H, Hasebe M (2009) ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 19:1327–1331

    CAS  PubMed  Google Scholar 

  • Muhammad I, Jing X-Q, Shalmani A, Ali M, Yi S, Gan P-F, Li W-Q, Liu W-T, Chen K-M (2018) Comparative in silico analysis of ferric reduction oxidase (FRO) genes expression patterns in response to abiotic stresses, metal and hormone applications. Molecules 23:1163

    PubMed Central  Google Scholar 

  • Ngo QA, Vogler H, Lituiev DS, Nestorova A, Grossniklaus U (2014) A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Dev Cell 29:491–500

    CAS  PubMed  Google Scholar 

  • Nguyen Q-N, Lee Y-S, Cho L-H, Jeong H-J, An G, Jung K-H (2015) Genome-wide identification and analysis of Catharanthus roseus RLK1-like kinases in rice. Planta 241:603–613

    CAS  PubMed  Google Scholar 

  • Nissen KS, Willats WG, Malinovsky FG (2016) Understanding CrRLK1L function: cell walls and growth control. Trends Plant Sci 21:516–527

    CAS  PubMed  Google Scholar 

  • Rounds CM, Bezanilla M (2013) Growth mechanisms in tip-growing plant cells. Annu Rev Plant Biol 64:243–265

    CAS  PubMed  Google Scholar 

  • Saifullah Bibi S, Waraich EA (2013) Effects of lead forms and organic acids on the growth and uptake of lead in hydroponically grown wheat. Commun Soil Sci Plant Anal 44:3150–3160

    CAS  Google Scholar 

  • Schallus T, Jaeckh C, Fehér K, Palma AS, Liu Y, Simpson JC, Mackeen M, Stier G, Gibson TJ, Feizi T (2008) Malectin: a novel carbohydrate-binding protein of the endoplasmic reticulum and a candidate player in the early steps of protein N-glycosylation. Mol Biol Cell 19:3404–3414

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci 95:5857–5864

    CAS  PubMed  Google Scholar 

  • Stephen Deslauriers, Paul Larsen (2010) FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Mol Plant 3:626–640

    Google Scholar 

  • Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699

    CAS  PubMed  Google Scholar 

  • Udomchalothorn T, Plaimas K, Comai L, Buaboocha T, Chadchawan S (2014) Molecular karyotyping and exome analysis of salt-tolerant rice mutant from somaclonal variation. Plant Genome. https://doi.org/10.3835/plantgenome2014.04.0016

    Article  Google Scholar 

  • Vaid N, Pandey PK, Tuteja N (2012) Genome-wide analysis of lectin receptor-like kinase family from Arabidopsis and rice. Plant Mol Biol 80:365–388

    CAS  PubMed  Google Scholar 

  • Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    CAS  PubMed  Google Scholar 

  • Wudick MM, Feijó JA (2014) At the intersection: merging Ca2+ and ROS signaling pathways in pollen. Mol Plant 7:1595–1597

    CAS  PubMed  Google Scholar 

  • Yang T, Wang L, Li C, Liu Y, Zhu S, Qi Y, Liu X, Lin Q, Luan S, Yu F (2015) Receptor protein kinase FERONIA controls leaf starch accumulation by interacting with glyceraldehyde-3-phosphate dehydrogenase. Biochem Biophys Res Commun 465:77–82

    CAS  PubMed  Google Scholar 

  • Yeh Y-H, Panzeri D, Kadota Y, Huang Y-C, Huang P-Y, Tao C-N, Roux M, Chien H-C, Chin T-C, Chu P-W (2016) The Arabidopsis malectin-like/LRR-RLK IOS1 is critical for BAK1-dependent and BAK1-independent pattern-triggered immunity. Plant Cell 00313:02016

    Google Scholar 

  • Yu F, Qian L, Nibau C, Duan Q, Kita D, Levasseur K, Li X, Lu C, Li H, Hou C (2012) FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc Natl Acad Sci 109(36):14693–14698

    CAS  PubMed  Google Scholar 

  • Yu F, Li J, Huang Y, Liu L, Li D, Chen L, Luan S (2014) FERONIA receptor kinase controls seed size in Arabidopsis thaliana. Mol Plant 7:920–922

    CAS  PubMed  Google Scholar 

  • Zhang M, Liu B (2017) Identification of a rice metal tolerance protein OsMTP11 as a manganese transporter. PLoS ONE 4:e0174987

    Google Scholar 

  • Zhang Q, Jia M, Xing Y, Qin L, Li B, Jia W (2016) Genome-wide identification and expression analysis of MRLK family genes associated with strawberry (Fragaria vesca) fruit ripening and abiotic stress responses. PLoS ONE 11:e0163647

    PubMed  PubMed Central  Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Evolutionary Divergence and Convergence in Proteins. Evolv Genes Proteins 97:97–166

    Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Nos. 31770204 and 31270299).

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  1. Xiu-Qing Jing, Abdullah Shalmani, and Meng-Ru Zhou have equally contributed to this work.

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  1. State Key Laboratory of Crop Stress Biology in Arid Area, College of Life Sciences, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Xiu-Qing Jing, Abdullah Shalmani, Meng-Ru Zhou, Peng-Tao Shi, Izhar Muhammad, Yi Shi, Rahat Sharif, Wen-Qiang Li, Wen-Ting Liu & Kun-Ming Chen

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  1. Xiu-Qing Jing
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Jing, XQ., Shalmani, A., Zhou, MR. et al. Genome-Wide Identification of Malectin/Malectin-Like Domain Containing Protein Family Genes in Rice and Their Expression Regulation Under Various Hormones, Abiotic Stresses, and Heavy Metal Treatments. J Plant Growth Regul 39, 492–506 (2020). https://doi.org/10.1007/s00344-019-09997-8

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