Genome-Wide Identification of PIN and PILS Gene Families in Areca catechu and the Potential Role of AcPIN6 in Lateral Brace Root Formation
Abstract
:1. Introduction
2. Results
2.1. Genome-Wide Identification of PIN and PILS Proteins in A. catechu
2.2. Chromosome Localization, Duplication, and Synteny of A. catechu PIN/PILS Genes
2.3. Analysis of Conserved Motifs and Gene Structures of A. catechu PIN/PILS Genes
2.4. Expression Profile of AcPIN/AcPILS Genes in Various Organs and Tissues
2.5. Expression Dynamics of AcPIN6 in Brace Roots during Various Growth Stages and in Different Parts of Brace Roots
2.6. PIN6 Is Specifically Expressed in Brace Roots of Palms
3. Discussion
4. Materials and Methods
4.1. Analysis of the PIN and PILS Gene Families
4.2. Phylogenetic Analysis of A. catechu PIN/PILS Gene Family
4.3. Chromosomal Distribution and Gene Synteny Analysis
4.4. Transmembrane Topology, Conserved Motifs, and Gene Structure Analysis of AcPINs/AcPILSs
4.5. Plant Materials and Treatment
4.6. RNA Extraction, cDNA Synthesis and Quantitative Real-Time PCR Analysis
4.7. Transformation of Arabidopsis
4.8. Subcellular Localization
4.9. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Peer, W.A.; Blakeslee, J.J.; Yang, H.; Murphy, A.S. Seven things we think we know about auxin transport. Mol. Plant. 2011, 4, 487–504. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.J.; Luo, J. The PIN-FORMED auxin efflux carriers in plants. Int. J. Mol. Sci. 2018, 19, 2759. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mravec, J.; Skůpa, P.; Bailly, A.; Hoyerová, K.; Krecek, P.; Bielach, A.; Petrásek, J.; Zhang, J.; Gaykova, V.; Stierhof, Y.D.; et al. Subcellular homeostasis of phytohormone auxin is mediated by the ER localized PIN5 transporter. Nature 2009, 459, 1136–1140. [Google Scholar] [CrossRef]
- Ding, Z.; Wang, B.; Moreno, I.; Dupláková, N.; Simon, S.; Carraro, N.; Reemmer, J.; Pěnčík, A.; Chen, X.; Tejos, R.; et al. ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat. Commun. 2012, 3, 941. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bennett, T.; Brockington, S.F.; Rothfels, C.; Graham, S.W.; Stevenson, D.; Kutchan, T.; Rolf, M.; Thomas, P.; Wong, G.K.; Leyser, O.; et al. Paralogous radiations of PIN proteins with multiple origins of noncanonical PIN structure. Mol. Biol. Evol. 2014, 31, 2042–2060. [Google Scholar] [CrossRef] [Green Version]
- Barbez, E.; Kubeš, M.; Rolčík, J.; Béziat, C.; Pěnčík, A.; Wang, B.; Rosquete, M.R.; Zhu, J.; Dobrev, P.I.; Lee, Y.; et al. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 2012, 485, 119–122. [Google Scholar] [CrossRef] [Green Version]
- Béziat, C.; Barbez, E.; Feraru, M.I.; Lucyshyn, D.; Kleine-Vehn, J. Light triggers PILS-dependent reduction in nuclear auxin signalling for growth transition. Nat. Plants 2017, 7, 706. [Google Scholar] [CrossRef]
- Sauer, M.; Kleine-Vehn, J. PIN-FORMED and PIN-LIKES auxin transport facilitators. Development 2019, 146, dev168088. [Google Scholar] [CrossRef] [Green Version]
- Cho, M.; Cho, H.T. The function of ABCB transporters in auxin transport. Plant Signal Behav. 2013, 8, e22990. [Google Scholar] [CrossRef] [Green Version]
- Péret, B.; Swarup, K.; Ferguson, A.; Seth, M.; Yang, Y.; Dhondt, S.; James, N.; Casimiro, I.; Perry, P.; Syed, A.; et al. AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell 2012, 24, 2874–2885. [Google Scholar] [CrossRef]
- Miyashita, Y.; Takasugi, T.; Ito, Y. Identification and expression analysis of PIN genes in rice. Plant Sci. 2010, 178, 424–428. [Google Scholar] [CrossRef]
- Forestan, C.; Farinati, S.; Varotto, S. The maize PIN gene family of auxin transporters. Front. Plant Sci. 2012, 3, 16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Feraru, E.; Vosolsobě, S.; Feraru, M.I.; Petrášek, J.; Kleine-Vehn, J. Evolution and structural diversification of PILS putative auxin carriers in plants. Front. Plant Sci. 2012, 3, 227. [Google Scholar] [PubMed] [Green Version]
- Frank, H.; Woong, J.P.; Michaela, S.; Katrin, W. From weeds to crops: Genetic analysis of root development in cereals. Trends Plant Sci. 2004, 9, 42–48. [Google Scholar]
- Hunter, I.R.; Bystriakova, N. Encyclopedia of Forest Sciences; Elsevier Academic Press: San Diego, SD, USA, 2004; pp. 1675–1681. [Google Scholar]
- Srimany, A.; George, C.; Naik, H.R.; Pinto, D.G.; Chandrakumar, N.; Pradeep, T. Development patterning and segregation of alkaloids in arece nut (seed of Areca catechu) revealed by magnetic resonance and mass spectrometry imaging. Phytochemistry 2016, 125, 35–42. [Google Scholar] [CrossRef]
- Peter, K.V.; Kurian, A.; Chopra, V.L. Encyclopedia of Applied Plant Sciences; Elsevier Academic Press: London, UK, 2003; pp. 956–960. [Google Scholar]
- Saini, S.; Sharma, I.; Kaur, N.; Pati, P.K. Auxin: A master regulator in plant root development. Plant Cell Rep. 2013, 32, 741–757. [Google Scholar] [CrossRef]
- Marhava, P.; Bassukas, A.E.L.; Zourelidou, M.; Kolb, M.; Moret, B.; Fastner, A.; Schulze, W.X.; Cattaneo, P.; Hammes, U.Z.; Schwechheimer, C.; et al. A molecular rheostat adjusts auxin flux to promote root protophloem differentiation. Nature 2018, 558, 297–300. [Google Scholar] [CrossRef]
- Balzan, S.; Johal, G.S.; Carraro, N. The role of auxin transporters in monocots development. Front Plant Sci. 2014, 5, 393. [Google Scholar] [CrossRef] [Green Version]
- Adamowski, M.; Friml, J. PIN-dependent auxin transport: Action, regulation, and evolution. Plant Cell 2015, 27, 20–32. [Google Scholar] [CrossRef] [Green Version]
- Wang, Y.Q.; Chai, C.L.; Valliyodan, B.; Maupin, C.; Annen, B.; Nguyen, H.T. Genome-wide analysis and expression profiling of the PIN auxin transporter gene family in soybean (Glycine max). BMC Genom. 2015, 16, 951. [Google Scholar] [CrossRef] [Green Version]
- Cazzonelli, C.I.; Vanstraelen, M.; Simon, S.; Yin, K.; Carron-Arthur, A.; Nisar, N.; Tarle, G.; Cuttriss, A.J.; Searle, I.R.; Benkova, E.; et al. Role of the Arabidopsis PIN6 auxin transporter in auxin homeostasis and auxin-mediated development. PLoS ONE 2013, 8, e70069. [Google Scholar] [CrossRef] [PubMed]
- Nisar, N.; Cuttriss, A.J.; Pogson, B.J.; Cazzonelli, C.I. The promoter of the Arabidopsis PIN6 auxin transporter enabled strong expression in the vasculature of roots, leaves, floral stems and reproductive organs. Plant Signal Behav. 2014, 9, e27898. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Simon, S.; Skůpa, P.; Viaene, T.; Zwiewka, M.; Tejos, R.; Klíma, P.; Čarná, M.; Rolčík, J.; De Rycke, R.; Moreno, I.; et al. PIN6 auxin transporter at endoplasmic reticulum and plasma membrane mediates auxin homeostasis and organogenesis in Arabidopsis. New Phytol. 2016, 211, 65–74. [Google Scholar] [CrossRef] [PubMed]
- Ditengou, F.A.; Gomes, D.; Nziengui, H.; Kochersperger, P.; Lasok, H.; Medeiros, V.; Paponov, I.A.; Nagy, S.K.; Nádai, T.V.; Mészáros, T.; et al. Characterization of auxin transporter PIN6 plasma membrane targeting reveals a function for PIN6 in plant bolting. New Phytol. 2017, 217, 1610–1624. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ganguly, A.; Lee, S.H.; Cho, M.; Lee, O.R.; Yoo, H.; Cho, H.T. Differential auxin-transporting activities of PIN-FORMED proteins in Arabidopsis root hair cells. Plant Physiol. 2010, 153, 1046–1061. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barbosa, I.C.R.; Schwechheimer, C. Dynamic control of auxin transport-dependent growth by AGCVIII protein kinases. Curr. Opin. Plant Biol. 2014, 22, 108–115. [Google Scholar] [CrossRef] [PubMed]
- Weller, B.; Zourelidou, M.; Frank, L.; Barbosa, I.C.; Fastner, A.; Richter, S.; Jürgens, G.; Hammes, U.Z.; Schwechheimer, C. Dynamic PIN-FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux-dependent growth. Proc. Natl. Acad. Sci. USA 2017, 114, E887–E896. [Google Scholar] [CrossRef] [Green Version]
- Zwiewka, M.; Bilanovičová, V.; Seifu, Y.W.; Nodzyński, T. The nuts and bolts of PIN auxin efflux carriers. Front. Plant Sci. 2019, 10, 985. [Google Scholar] [CrossRef] [Green Version]
- Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 2020, 13, 1194–1202. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wang, Y.; Zhou, G.; Luo, H.; Li, X.; Zhang, K.; Wan, Y. Genome-Wide Identification of PIN and PILS Gene Families in Areca catechu and the Potential Role of AcPIN6 in Lateral Brace Root Formation. Plants 2023, 12, 33. https://doi.org/10.3390/plants12010033
Wang Y, Zhou G, Luo H, Li X, Zhang K, Wan Y. Genome-Wide Identification of PIN and PILS Gene Families in Areca catechu and the Potential Role of AcPIN6 in Lateral Brace Root Formation. Plants. 2023; 12(1):33. https://doi.org/10.3390/plants12010033
Chicago/Turabian StyleWang, Yicheng, Guangzhen Zhou, Haifen Luo, Xinyu Li, Kelan Zhang, and Yinglang Wan. 2023. "Genome-Wide Identification of PIN and PILS Gene Families in Areca catechu and the Potential Role of AcPIN6 in Lateral Brace Root Formation" Plants 12, no. 1: 33. https://doi.org/10.3390/plants12010033