Abstract
Main conclusion
Genome-wide identification, together with gene expression patterns and promoter region analysis of FYVE and PHOX proteins in Physcomitrella patens, emphasized their importance in regulating mainly developmental processes in P. patens.
Abstract
Phosphatidylinositol 3-phosphate (PtdIns3P) is a signaling phospholipid, which regulates several aspects of plant growth and development, as well as responses to biotic and abiotic stresses. The mechanistic insights underlying PtdIns3P mode of action, specifically through effector proteins have been partially explored in plants, with main focus on Arabidopsis thaliana. In this study, we searched for genes coding for PtdIns3P-binding proteins such as FYVE and PHOX domain-containing sequences from different photosynthetic organisms to gather evolutionary insights on these phosphoinositide binding domains, followed by an in silico characterization of the FYVE and PHOX gene families in the moss Physcomitrella patens. Phylogenetic analysis showed that PpFYVE proteins can be grouped in 7 subclasses, with an additional subclass whose FYVE domain was lost during evolution to higher plants. On the other hand, PpPHOX proteins are classified into 5 subclasses. Expression analyses based on RNAseq data together with the analysis of cis-acting regulatory elements and transcription factor (TF) binding sites in promoter regions suggest the importance of these proteins in regulating stress responses but mainly developmental processes in P. patens. The results provide valuable information and robust candidate genes for future functional analysis aiming to further explore the role of this signaling pathway mainly during growth and development of tip growing cells and during the transition from 2 to 3D growth. These studies would identify ancestral regulatory players undertaken during plant evolution.
Similar content being viewed by others
Abbreviations
- BRX:
-
Brevis radix domain
- ESCRT:
-
Endosomal sorting complex required for transport
- PH:
-
Plekstrin homology domain
- PPIs:
-
Phosphoinositides
- PtdIns3P :
-
Phosphatidylinositol 3-phosphate
- PtdIns(3,5)P2 :
-
Phosphatidylinositol 3,5-bisphosphate
- SNX:
-
Sorting nexin
- TF:
-
Transcription factor
References
Aoyama T, Hiwatashi Y, Shigyo M, Kofuji R, Kubo M, Ito M, Hasebe M (2012) AP2-type transcription factors determine stem cell identity in the moss Physcomitrella patens. Development 139:3120–3129. https://doi.org/10.1242/dev.076091
Bader GD, Hogue CW (2003) An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics 4:2
Bak G, Lee EJ, Lee Y, Kato M, Segami S, Sze H, Maeshima M, Hwang JU (2013) Rapid structural changes and acidification of guard cell vacuoles during stomatal closure require phosphatidylinositol 3,5-bisphosphate. Plant Cell 25:2202–2216. https://doi.org/10.1105/tpc.113.110411
Banerjee S, Basu S, Sarkar S (2010) Comparative genomics reveals selective distribution and domain organization of FYVE and PX domain proteins across eukaryotic lineages. BMC Genomics 11:83. https://doi.org/10.1186/1471-2164-11-83
Barberon M, Dubeaux G, Kolb C, Isono E, Zelazny E, Vert G (2014) Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis. Proc Natl Acad Sci USA 111:8293–8298. https://doi.org/10.1073/pnas.1402262111
Bechtold U, Field B (2018) Molecular mechanisms controlling plant growth during abiotic stress. J Exp Bot 69:2753–2758. https://doi.org/10.1093/jxb/ery157
Beuchat J, Scacchi E, Tarkowska D, Ragni L, Strnad M, Hardtke CS (2010) BRX promotes Arabidopsis shoot growth. New Phytol 188:23–29. https://doi.org/10.1111/j.1469-8137.2010.03387.x
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bravo J, Karathanassis D, Pacold CM, Pacold ME, Ellson CD, Anderson KE, Butler PJ, Lavenir I et al (2001) The crystal structure of the PX domain from p40(phox) bound to phosphatidylinositol 3-phosphate. Mol Cell 8:829–839
Bray NL, Pimentel H, Melsted P, Pachter L (2016) Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol 34:525–527. https://doi.org/10.1038/nbt.3519
Briggs GC, Mouchel CF, Hardtke CS (2006) Characterization of the plant-specific BREVIS RADIX gene family reveals limited genetic redundancy despite high sequence conservation. Plant Physiol 140:1306–1316. https://doi.org/10.1104/pp.105.075382
Brumbarova T, Ivanov R (2016) Differential gene expression and protein phosphorylation as factors regulating the state of the Arabidopsis SNX1 protein complexes in response to environmental stimuli. Front Plant Sci 7:1456. https://doi.org/10.3389/fpls.2016.01456
Buckley CM, Heath VL, Guého A, Bosmani C, Knobloch P, Sikakana P, Personnic N, Dove SK et al (2019) PIKfyve/Fab1 is required for efficient V-ATPase and hydrolase delivery to phagosomes, phagosomal killing, and restriction of Legionella infection. PLoS Pathog 15:e1007551. https://doi.org/10.1371/journal.ppat.1007551
Capella M, Ribone PA, Chan RL (2015) Functional characterization of the homeodomain leucine zipper I transcription factor AtHB13 reveals a crucial role in Arabidopsis development. J Exp Bot 66:5929–5943. https://doi.org/10.1093/jxb/erv302
Chandra M, Chin YK, Mas C, Feathers JR, Paul B, Datta S, Chen KE, Jia X et al (2019) Classification of the human phox homology (PX) domains based on their phosphoinositide binding specificities. Nat Commun 10:1528. https://doi.org/10.1038/s41467-019-09355-y
Collonnier C, Epert A, Mara K, Maclot F, Guyon-Debast A, Charlot F, White C, Schaefer DG et al (2016) CRISPR-Cas9 mediated efficient directed mutagenesis and RAD51-dependent and -independent gene targeting in the moss Physcomitrella patens. Plant Biotechnol J 15:122–131. https://doi.org/10.1111/pbi.12596
Estrada-Navarrete G, Cruz-Mireles N, Lascano R, Alvarado-Affantranger X, Hernàndez A, Barraza A, Olivares JE, Arthikala MK et al (2016) An autophagy-related kinase is essential for the symbiotic relationship between Phaseolus vulgaris and both rhizobia and arbuscular mycorrhizal fungi. Plant Cell 28(9):2326–2341. https://doi.org/10.1105/tpc.15.01012
Filimonenko M, Isakson P, Finley KD, Anderson M, Jeong H, Melia TJ, Bartlett BJ, Myers KM et al (2010) The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein Alfy. Mol Cell 38:265–279. https://doi.org/10.1016/j.molcel.2010.04.007
Frank MH, Scanlon MJ (2015) Cell-specific transcriptomic analyses of three-dimensional shoot development in the moss Physcomitrella patens. Plant J 83:743–751. https://doi.org/10.1111/tpj.12928
Franssen HJ, Xiao TT, Kulikova O, Wan X, Bisseling T, Scheres B, Heidstra R (2015) Root developmental programs shape the Medicago truncatula nodule meristem. Development 142:2941–2950. https://doi.org/10.1242/dev.120774
Gao C, Luo M, Zhao Q, Yang R, Cui Y, Zeng Y, Xia J, Jiang L (2014) A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth. Curr Biol 24:2556–2563. https://doi.org/10.1016/j.cub.2014.09.014
Gao C, Zhuang X, Cui Y, Fu X, He Y, Zhao Q, Zeng Y, Shen J et al (2015) Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation. Proc Natl Acad Sci USA 112:1886–1891. https://doi.org/10.1073/pnas.1421271112
Gaullier JM, Ronning E, Gillooly DJ, Stenmark H (2000) Interaction of the EEA1 FYVE finger with phosphatidylinositol 3-phosphate and early endosomes. Role of conserved residues. J Biol Chem 275:24595–24600. https://doi.org/10.1074/jbc.M906554199
Gel B, Serra E (2017) karyoploteR: an R/Bioconductor package to plot customizable genomes displaying arbitrary data. Bioinformatics 33:3088–3090. https://doi.org/10.1093/bioinformatics/btx346
Gerth K, Lin F, Menzel W, Krishnamoorthy P, Stenzel I, Heilmann M, Heilmann I (2017) Guilt by association: a phenotype-based view of the plant phosphoinositide network. Annu Rev Plant Biol 68:349–374. https://doi.org/10.1146/annurev-arplant-042916-041022
Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, Parton RG, Stenmark H (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 19:4577–4588. https://doi.org/10.1093/emboj/19.17.4577
Hadjebi O, Casas-Terradellas E, Garcia-Gonzalo FR, Rosa JL (2008) The RCC1 superfamily: from genes, to function, to disease. Biochim Biophys Acta 1783:1467–1479. https://doi.org/10.1016/j.bbamcr.2008.03.015
Hanzawa T, Shibasaki K, Numata T, Kawamura Y, Gaude T, Rahman A (2013) Cellular auxin homeostasis under high temperature is regulated through a sorting NEXIN1-dependent endosomal trafficking pathway. Plant Cell 25:3424–3433. https://doi.org/10.1105/tpc.113.115881
Heucken N, Ivanov R (2018) The retromer, sorting nexins and the plant endomembrane protein trafficking. J Cell Sci. https://doi.org/10.1242/jcs.203695
Hirano T, Matsuzawa T, Takegawa K, Sato MH (2011) Loss-of-function and gain-of-function mutations in FAB1A/B impair endomembrane homeostasis, conferring pleiotropic developmental abnormalities in Arabidopsis. Plant Physiol 155:797–807. https://doi.org/10.1104/pp.110.167981
Hirano T, Munnik T, Sato MH (2015) Phosphatidylinositol 3-phosphate 5-kinase, FAB1/PIKfyve kinase mediates endosome maturation to establish endosome-cortical microtubule interaction in Arabidopsis. Plant Physiol 169:1961–1974. https://doi.org/10.1104/pp.15.01368
Hirano T, Munnik T, Sato MH (2017) Inhibition of phosphatidylinositol 3,5-bisphosphate production has pleiotropic effects on various membrane trafficking routes in Arabidopsis. Plant Cell Physiol 58:120–129. https://doi.org/10.1093/pcp/pcw164
Hopkins J, Pierre O, Kazmierczak T, Gruber V, Frugier F, Clement M, Frendo P, Herouart D et al (2014) MtZR1, a PRAF protein, is involved in the development of roots and symbiotic root nodules in Medicago truncatula. Plant Cell Environ 37:658–669. https://doi.org/10.1111/pce.12185
Horstman A, Fukuoka H, Muino JM, Nitsch L, Guo C, Passarinho P, Sanchez-Perez G, Immink R et al (2015) AIL and HDG proteins act antagonistically to control cell proliferation. Development 142:454. https://doi.org/10.1242/dev.117168
Ivanov R, Brumbarova T, Blum A, Jantke AM, Fink-Straube C, Bauer P (2014) SORTING NEXIN1 is required for modulating the trafficking and stability of the Arabidopsis IRON-REGULATED TRANSPORTER1. Plant Cell 26:1294–1307. https://doi.org/10.1105/tpc.113.116244
Jaillais Y, Fobis-Loisy I, Miège C, Rollin C, Gaude T (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443:106–109. https://doi.org/10.1038/nature05046
Jensen RB, La Cour T, Albrethsen J, Nielsen M, Skriver K (2001) FYVE zinc-finger proteins in the plant model Arabidopsis thaliana: identification of PtdIns3P-binding residues by comparison of classic and variant FYVE domains. Biochem J 359:165–173
Joo JH, Yoo HJ, Hwang I, Lee JS, Nam KH, Bae YS (2005) Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3-kinase. FEBS Lett 579:1243–1248. https://doi.org/10.1016/j.febslet.2005.01.018
Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A, Arredondo FD, Hanlon R et al (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284–295. https://doi.org/10.1016/j.cell.2010.06.008
Kutateladze TG (2006) Phosphatidylinositol 3-phosphate recognition and membrane docking by the FYVE domain. Biochim Biophys Acta 1761:868–877. https://doi.org/10.1016/j.bbalip.2006.03.011
Lee Y, Bak G, Choi Y, Chuang WI, Cho HT (2008a) Roles of phosphatidylinositol 3-kinase in root hair growth. Plant Physiol 147:624–635. https://doi.org/10.1104/pp.108.117341
Lee Y, Kim ES, Choi Y, Hwang I, Staiger CJ, Chung YY (2008b) The Arabidopsis phosphatidylinositol 3-kinase is important for pollen development. Plant Physiol 147:1886–1897. https://doi.org/10.1104/pp.108.121590
Leprince AS, Magalhaes N, De Vos D, Bordenave M, Crilat E, Clément G, Meyer C, Munnik T et al (2014) Involvement of phosphatidylinositol 3-kinase in the regulation of proline catabolism in Arabidopsis thaliana. Front Plant Sci 5:772. https://doi.org/10.3389/fpls.2014.00772
Leshem Y, Seri L, Levine A (2007) Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J 51:185–197. https://doi.org/10.1111/j.1365-313X.2007.03134.x
Meijer HJG, Divecha N, van den Ende H, Musgrave A, Munnik T (1999) Hyperosmotic stress induces rapid synthesis of phosphatidyl-d-inositol 3,5-bisphosphate in plant cells. Planta 208:294–298. https://doi.org/10.1007/s004250050561
Moravcevic K, Oxley CL, Lemmon MA (2012) Conditional peripheral membrane proteins: facing up to limited specificity. Structure 20:15–27. https://doi.org/10.1016/j.str.2011.11.012
Moreno-Risueno MA, Sozzani R, Yardımcı GG, Petricka JJ, Vernoux T, Blilou I, Alonso J, Winter CM et al (2015) Transcriptional control of tissue formation throughout root development. Science 350:426–430. https://doi.org/10.1126/science.aad1171
Mouchel CF, Briggs GC, Hardtke CS (2004) Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev 18:700–714. https://doi.org/10.1101/gad.1187704
Mukae K, Inoue Y, Moriyasu Y (2015) ATG5-knockout mutants of Physcomitrella provide a platform for analyzing the involvement of autophagy in senescence processes in plant cells. Plant Signal Behav 10:e1086859. https://doi.org/10.1080/15592324.2015.1086859
Noack LC, Jaillais Y (2017) Precision targeting by phosphoinositides: how PIs direct endomembrane trafficking in plants. Curr Opin Plant Biol 40:22–33. https://doi.org/10.1016/j.pbi.2017.06.017
Ortiz-Ramírez C, Hernandez-Coronado M, Thamm A, Catarino B, Wang M, Dolan L, Feijó JA, Becker JD (2016) A transcriptome atlas of Physcomitrella patens provides insights into the evolution and development of land plants. Mol Plant 9:205–220. https://doi.org/10.1016/j.molp.2015.12.002
Phan NQ, Kim SJ, Bassham DC (2008) Overexpression of Arabidopsis sorting nexin AtSNX2b inhibits endocytic trafficking to the vacuole. Mol Plant 1:961–976. https://doi.org/10.1093/mp/ssn057
Pourcher M, Santambrogio M, Thazar N, Thierry AM, Fobis-Loisy I, Miège C, Jaillais Y, Gaude T (2010) Analyses of sorting nexins reveal distinct retromer-subcomplex functions in development and protein sorting in Arabidopsis thaliana. Plant Cell 22:3980–3991. https://doi.org/10.1105/tpc.110.078451
Rensing SA (2017) Why we need more non-seed plant models. New Phytol 216:355–360. https://doi.org/10.1111/nph.14464
Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69. https://doi.org/10.1126/science.1150646
Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:e47. https://doi.org/10.1093/nar/gkv007
Robert G, Muñoz N, Alvarado-Affantranger X, Saavedra L, Davidenco V, Rodríguez-Kessler M, Estrada-Navarrete G, Sánchez F et al (2018) Phosphatidylinositol 3-kinase at the very early symbiont perception: a local nodulation control under stress conditions? J Exp Bot 69(8):2037–2048. https://doi.org/10.1093/jxb/ery030
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
Saavedra L, Balbi V, Dove SK, Hiwatashi Y, Mikami K, Sommarin M (2009) Characterization of phosphatidylinositol phosphate kinases from the moss Physcomitrella patens: PpPIPK1 and PpPIPK2. Plant Cell Physiol 50:595–609. https://doi.org/10.1093/pcp/pcp018
Saavedra L, Catarino R, Heinz T, Heilmann I, Bezanilla M, Malhó R (2015) Phosphatase and tensin homolog is a growth repressor of both rhizoid and gametophore development in the moss Physcomitrella patens. Plant Physiol 169:2572–2586. https://doi.org/10.1104/pp.15.01197
Saddic LA, Huvermann B, Bezhani S, Su Y, Winter CM, Kwon CS, Collum RP, Wagner D (2006) The LEAFY target LMI1 is a meristem identity regulator and acts together with LEAFY to regulate expression of CAULIFLOWER. Development 133:1673. https://doi.org/10.1242/dev.02331
Sakurai HT, Inoue T, Nakano A, Ueda T (2016) ENDOSOMAL RAB EFFECTOR WITH PX-DOMAIN, an interacting partner of RAB5 GTPases, regulates membrane trafficking to protein storage vacuoles in Arabidopsis. Plant Cell 28:1490–1503. https://doi.org/10.1105/tpc.16.00326
Schaefer DG, Zrÿd JP (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206
Schink KO, Raiborg C, Stenmark H (2013) Phosphatidylinositol 3-phosphate, a lipid that regulates membrane dynamics, protein sorting and cell signalling. BioEssays 35:900–912. https://doi.org/10.1002/bies.201300064
Schink KO, Tan KW, Stenmark H (2016) Phosphoinositides in control of membrane dynamics. Annu Rev Cell Dev Biol 32:143–171. https://doi.org/10.1146/annurev-cellbio-111315-125349
Seet LF, Hong W (2006) The Phox (PX) domain proteins and membrane traffic. Biochim Biophys Acta 1761:878–896. https://doi.org/10.1016/j.bbalip.2006.04.011
Serrazina S, Dias FV, Malhó R (2014) Characterization of FAB1 phosphatidylinositol kinases in Arabidopsis pollen tube growth and fertilization. New Phytol 203:784–793. https://doi.org/10.1111/nph.12836
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
Simonsen A, Birkeland HC, Gillooly DJ, Mizushima N, Kuma A, Yoshimori T, Slagsvold T, Brech A et al (2004) Alfy, a novel FYVE-domain-containing protein associated with protein granules and autophagic membranes. J Cell Sci 117:4239–4251. https://doi.org/10.1242/jcs.01287
Son O, Cho HY, Kim MR, Lee H, Lee MS, Song E, Park JH, Nam KH et al (2005) Induction of a homeodomain-leucine zipper gene by auxin is inhibited by cytokinin in Arabidopsis roots. Biochem Biophys Res Commun 326:203–209. https://doi.org/10.1016/j.bbrc.2004.11.014
Stevenson SR, Kamisugi Y, Trinh CH, Schmutz J, Jenkins JW, Grimwood J, Muchero W, Tuskan GA et al (2016) Genetic analysis of Physcomitrella patens identifies ABSCISIC ACID NON-RESPONSIVE, a regulator of ABA responses unique to basal land plants and required for desiccation tolerance. Plant Cell 28:1310–1327. https://doi.org/10.1105/tpc.16.00091
Sutipatanasomboon A, Herberth S, Alwood EG, Häweker H, Müller B, Shahriari M, Zienert AY, Marin B et al (2017) Disruption of the plant-specific CFS1 gene impairs autophagosome turnover and triggers EDS1-dependent cell death. Sci Rep 7:8677. https://doi.org/10.1038/s41598-017-08577-8
Thelander M, Landberg K, Sundberg E (2018) Auxin-mediated developmental control in the moss Physcomitrella patens. J Exp Bot 69:277–290. https://doi.org/10.1093/jxb/erx255
van Gisbergen PA, Li M, Wu SZ, Bezanilla M (2012) Class II formin targeting to the cell cortex by binding PI(3,5)P2 is essential for polarized growth. J Cell Biol 198:235–250. https://doi.org/10.1083/jcb.201112085
van Leeuwen W, Okrész L, Bögre L, Munnik T (2004) Learning the lipid language of plant signalling. Trends Plant Sci 9:378–384. https://doi.org/10.1016/j.tplants.2004.06.008
Vidali L, Bezanilla M (2012) Physcomitrella patens: a model for tip cell growth and differentiation. Curr Opin Plant Biol 15:625–631. https://doi.org/10.1016/j.pbi.2012.09.008
Wywial E, Singh SM (2010) Identification and structural characterization of FYVE domain-containing proteins of Arabidopsis thaliana. BMC Plant Biol 10:157. https://doi.org/10.1186/1471-2229-10-157
Xiao L, Wang H, Wan P, Kuang T, He Y (2011) Genome-wide transcriptome analysis of gametophyte development in Physcomitrella patens. BMC Plant Biol 11:177. https://doi.org/10.1186/1471-2229-11-177
Xiao L, Zhang L, Yang G, Zhu H, He Y (2012) Transcriptome of protoplasts reprogrammed into stem cells in Physcomitrella patens. PLoS ONE 7:e35961. https://doi.org/10.1371/journal.pone.0035961
Xiao S, Shao M, Dong W, Li WQ, Liu FQ (2016) Identification and evolution of FYVE domain-containing proteins and their expression patterns in response to abiotic stresses in rice. Plant Mol Biol Rep 34:1064–1082. https://doi.org/10.1007/s11105-016-0988-9
Zhuang X, Jiang L (2014) Autophagosome biogenesis in plants: roles of SH3P2. Autophagy 10:704–705. https://doi.org/10.4161/auto.28060
Acknowledgements
This work was supported by grants from the Agencia Nacional de Promoción Científica y Tecnológica, Argentina (FONCYT-PICT-2016-0497), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET-PIP2015-11220150100818CO) and Secretaría de Ciencia y Tecnología (SECYT), Universidad Nacional de Córdoba (UNC). Additional funding was provided by the Portuguese Foundation for Science and Technology (PTDC/ASP-HOR/28485/2017), and UID/MULTI/04046/2019 Research Unit grant from FCT to BioISI.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Fig. S1
Summary of statistics of the several RNA sequencing studies assessed here. a Mean Quality Scores graphic. Lines in green represent each library with quality score > 20 Phred Score. b Barplot shows the library fragment size before (pink) and after (blue) trimming. c Barplot depicts the number of reads by library before (pink) and after (blue) trimming. d Stacked barplot summarizes the percentage of mapped (pink) and unmapped (blue) reads by library from the pseudo-bam files obtained by Kallisto (Bray et al. 2016) (PDF 552 kb)
Fig. S2
Sequence alignment and motif analysis of the FYVE domain of the repertory of FYVE proteins in P. patens and A. thaliana (PDF 995 kb)
Fig. S3
Sequence alignment and motif analysis of the PHOX domain of the repertory of PHOX proteins in P. patens and A. thaliana (PDF 1239 kb)
Table S1
FYVE and PHOX genes used in this study (XLSX 20 kb)
Table S2
PpFYVE and PpPHOX promoter cis-acting regulatory elements analyzed with PlantCARE (XLSX 12 kb)
Table S3
PpFYVE and PpPHOX promoter transcription factor binding sites analyzed with PlantPAN2.0 (XLSX 24 kb)
Table S4
Scoring tables of the known motif analysis (Homer v4.977) of PpFYVE genes (XLSX 1466 kb)
Table S5
Scoring tables of the known motif analysis (Homer v4.977) of PpPHOX genes (XLSX 572 kb)
Table S6
Interaction network analysis of the known motifs of the PpPHOX and PpFYVE genes in Cytoscape (v3.6.1). a Motif-gene interaction network file of PpPHOX genes. b Node-scoring table of PpPHOX net build by Molecular Complex Detection (MCODE) App. c Motif-gene interaction network file of PpFYVE genes. d Node-scoring table of PpFYVE net build by MCODE (XLS 1067 kb)
Table S7
Bioproject list of the transcriptomic studies in Physcomitrella patens surveyed on the SRA and GEO databases from the NCBI website (XLSX 52 kb)
Table S8
PpFYVE intron–exon structure (XLSX 22 kb)
Table S9
PpPHOX intron–exon structure (DOCX 2840 kb)
Table S10
Pfam scan phospholipases D (PLDs) (DOCX 2274 kb)
Rights and permissions
About this article
Cite this article
Agudelo-Romero, P., Fortes, A.M., Suárez, T. et al. Evolutionary insights into FYVE and PHOX effector proteins from the moss Physcomitrella patens. Planta 251, 62 (2020). https://doi.org/10.1007/s00425-020-03354-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-020-03354-w