Dissecting Hierarchies between Light, Sugar and Auxin Action Underpinning Root and Root Hair Growth
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
19-13375Y
Grantová Agentura České Republiky
CZ.02.1.01/0.0/0.0/16_019/0000738
Ministerstvo Školství, Mládeže a Tělovýchovy
PubMed
33430437
PubMed Central
PMC7826589
DOI
10.3390/plants10010111
PII: plants10010111
Knihovny.cz E-zdroje
- Klíčová slova
- PIN-FORMED2, dark grown roots, gravitropic index, light grown roots, root growth, root hair, root hair elongation, shootward auxin transport, sucrose, sugar, total root length,
- Publikační typ
- časopisecké články MeSH
Plant roots are very plastic and can adjust their tissue organization and cell appearance during abiotic stress responses. Previous studies showed that direct root illumination and sugar supplementation mask root growth phenotypes and traits. Sugar and light signaling where further connected to changes in auxin biosynthesis and distribution along the root. Auxin signaling underpins almost all processes involved in the establishment of root traits, including total root length, gravitropic growth, root hair initiation and elongation. Root hair plasticity allows maximized nutrient uptake and therefore plant productivity, and root hair priming and elongation require proper auxin availability. In the presence of sucrose in the growth medium, root hair emergence is partially rescued, but the full potential of root hair elongation is lost. With our work we describe a combinatory study showing to which extent light and sucrose are antagonistically influencing root length, but additively affecting root hair emergence and elongation. Furthermore, we investigated the impact of the loss of PIN-FORMED2, an auxin efflux carrier mediating shootward auxin transporter, on the establishment of root traits in combination with all growth conditions.
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Silva-Navas J., Moreno-Risueno M.A., Manzano C., Pallero-Baena M., Navarro-Neila S., Téllez-Robledo B., Garcia-Mina J.M., Baigorri R., Gallego F.J., Del Pozo J.C. D-Root: A System for Cultivating Plants with the Roots in Darkness or under Different Light Conditions. Plant J. 2015;84:244–255. doi: 10.1111/tpj.12998. PubMed DOI
Barrada A., Montané M.H., Robaglia C., Menand B. Spatial Regulation of Root Growth: Placing the Plant TOR Pathway in a Developmental Perspective. Int. J. Mol. Sci. 2015;196:19671–19697. doi: 10.3390/ijms160819671. PubMed DOI PMC
Van Gelderen K., Kang C., Pierik R. Light Signaling, Root Development, and Plasticity. Plant Physiol. 2018;176:1049–1060. doi: 10.1104/pp.17.01079. PubMed DOI PMC
Korver R.A., Koevoets I.T., Testerink C. Out of Shape during Stress: A Key Role for Auxin. Trends Plant Sci. 2018;23:783–793. doi: 10.1016/j.tplants.2018.05.011. PubMed DOI PMC
Kleine-Vehn J., Leitner J., Zwiewka M., Sauer M., Abas L., Luschnig C., Friml J. Differential Degradation of PIN2 Auxin Efflux Carrier by Retromer-Dependent Vacuolar Targeting. Proc. Natl. Acad. Sci. USA. 2008;105:17812–17817. doi: 10.1073/pnas.0808073105. PubMed DOI PMC
Gallei M., Luschnig C., Friml J. Auxin Signalling in Growth: Schrödinger’s Cat out of the Bag. Curr. Opin. Plant Biol. 2020;53:43–49. doi: 10.1016/j.pbi.2019.10.003. PubMed DOI
Qi J., Greb T. Cell Polarity in Plants: The Yin and Yang of Cellular Functions. Curr. Opin. Plant Biol. 2017;35:105–110. doi: 10.1016/j.pbi.2016.11.015. PubMed DOI PMC
Bailey-Serres J., Pierik R., Ruban A., Wingler A. The Dynamic Plant: Capture, Transformation, and Management of Energy. Plant Physiol. 2018 doi: 10.1104/pp.18.00041. PubMed DOI PMC
Sairanen I., Novák O., Pěnčík A., Ikeda Y., Jones B., Sandberg G., Ljung K. Soluble Carbohydrates Regulate Auxin Biosynthesis via PIF Proteins in Arabidopsis. Plant Cell. 2013;24:4907–4916. doi: 10.1105/tpc.112.104794. PubMed DOI PMC
Retzer K., Korbei B., Luschnig C. Auxin and Its Role in Plant Development. Springer; Vienna, Austria: 2014. Auxin and Tropisms. DOI
Retzer K., Akhmanova M., Konstantinova N., Malínská K., Leitner J., Petrášek J., Luschnig C. Brassinosteroid Signaling Delimits Root Gravitropism via Sorting of the Arabidopsis PIN2 Auxin Transporter. Nat. Commun. 2019;10:1–15. doi: 10.1038/s41467-019-13543-1. PubMed DOI PMC
Pierik R., Testerink C. The Art of Being Flexible: How to Escape from Shade, Salt, and Drought1. Plant Physiol. 2014;166:5–22. doi: 10.1104/pp.114.239160. PubMed DOI PMC
De Smet I. Lateral Root Initiation: One Step at a Time. New Phytol. 2012;193:867–873. doi: 10.1111/j.1469-8137.2011.03996.x. PubMed DOI
Orman-Ligeza B., Parizot B., Gantet P.P., Beeckman T., Bennett M.J., Draye X. Post-Embryonic Root Organogenesis in Cereals: Branching out from Model Plants. Trends Plant Sci. 2013;18:459–467. doi: 10.1016/j.tplants.2013.04.010. PubMed DOI
Leyser O. Auxin Signaling. Plant Physiol. 2018 doi: 10.1104/pp.17.00765. PubMed DOI PMC
Lavenus J., Goh T., Roberts I., Guyomarc’h S., Lucas M., De Smet I., Fukaki H., Beeckman T., Bennett M., Laplaze L. Lateral Root Development in Arabidopsis: Fifty Shades of Auxin. Trends Plant Sci. 2013;18:450–458. doi: 10.1016/j.tplants.2013.04.006. PubMed DOI
Baldwin K.L., Strohm A.K., Masson P.H. Gravity Sensing and Signal Transduction in Vascular Plant Primary Roots. Am. J. Bot. 2013;100:126–142. doi: 10.3732/ajb.1200318. PubMed DOI
Band L.R., Wells D.M., Larrieu A., Sun J., Middleton A.M., French A.P., Brunoud G., Sato E.M., Wilson M.H., Peŕet B., et al. Root Gravitropism Is Regulated by a Transient Lateral Auxin Gradient Controlled by a Tipping-Point Mechanism. Proc. Natl. Acad. Sci. USA. 2012;109:4668–4673. doi: 10.1073/pnas.1201498109. PubMed DOI PMC
Scheuring D., Löfke C., Krüger F., Kittelmann M., Eisa A., Hughes L., Smith R.S., Hawes C., Schumacher K., Kleine-Vehn J. Actin-Dependent Vacuolar Occupancy of the Cell Determines Auxin-Induced Growth Repression. Proc. Natl. Acad. Sci. USA. 2016;113:452–457. doi: 10.1073/pnas.1517445113. PubMed DOI PMC
Liu M., Chen Y., Chen Y., Shin J.-H., Mila I., Audran C., Zouine M., Pirrello J., Bouzayen M. The Tomato Ethylene Response Factor Sl-ERF.B3 Integrates Ethylene and Auxin Signaling via Direct Regulation of Sl-Aux/IAA27. New Phytol. 2018;219:631–640. doi: 10.1111/nph.15165. PubMed DOI
Silva-Navas J., Moreno-Risueno M.A., Manzano C., Téllez-Robledo B., Navarro-Neila S., Carrasco V., Pollmann S., Gallego F.J., Del Pozo J.C. Flavonols Mediate Root Phototropism and Growth through Regulation of Proliferation-to-Differentiation Transition. Plant Cell. 2016;28:1372–1387. doi: 10.1105/tpc.15.00857. PubMed DOI PMC
Silva-Navas J., Conesa C.M., Saez A., Navarro-Neila S., Garcia-Mina J.M., Zamarreño A.M., Baigorri R., Swarup R., del Pozo J.C. Role of Cis-Zeatin in Root Responses to Phosphate Starvation. New Phytol. 2019;224:242–257. doi: 10.1111/nph.16020. PubMed DOI
Retzer K., Lacek J., Skokan R., Del Genio C.I., Vosolsobě S., Laňková M., Malínská K., Konstantinova N., Zažímalová E., Napier R.M., et al. Evolutionary Conserved Cysteines Function as Cis-Acting Regulators of Arabidopsis PIN-FORMED 2 Distribution. Int. J. Mol. Sci. 2017;18:2274. doi: 10.3390/ijms18112274. PubMed DOI PMC
Tomanov K., Luschnig C., Bachmair A. Ubiquitin Lys 63 Chains-Second-Most Abundant, but Poorly Understood in Plants. Front. Plant Sci. 2014;5:15. doi: 10.3389/fpls.2014.00015. PubMed DOI PMC
Halat L.S., Gyte K., Wasteneys G.O. Microtubule-Associated Protein CLASP Is Translationally Regulated in Light-Dependent Root Apical Meristem Growth. Plant Physiol. 2020 doi: 10.1104/pp.20.00474. PubMed DOI PMC
Ötvös K., Marconi M., Vega A., O’ Brien J., Johnson A., Abualia R., Antonielli L., Montesinos J.C., Zhang Y., Tan S., et al. Modulation of Root Growth by Nutrient-Defined Fine-Tuning of Polar Auxin Transport. bioRxiv. 2020 doi: 10.1101/2020.06.19.160994. PubMed DOI PMC
Tan S., Zhang X., Kong W., Yang X.L., Molnár G., Vondráková Z., Filepová R., Petrášek J., Friml J., Xue H.W. The Lipid Code-Dependent Phosphoswitch PDK1–D6PK Activates PIN-Mediated Auxin Efflux in Arabidopsis. Nat. Plants. 2020:1–14. doi: 10.1038/s41477-020-0648-9. PubMed DOI
Korbei B., Moulinier-Anzola J., De-Araujo L., Lucyshyn D., Retzer K., Khan M.A., Luschnig C. Arabidopsis TOL Proteins Act as Gatekeepers for Vacuolar Sorting of PIN2 Plasma Membrane Protein. Curr. Biol. 2013;23:2500–2505. doi: 10.1016/j.cub.2013.10.036. PubMed DOI
Laxmi A., Pan J., Morsy M., Chen R. Light Plays an Essential Role in Intracellular Distribution of Auxin Efflux Carrier PIN2 in Arabidopsis Thaliana. PLoS ONE. 2008;3:e1510. doi: 10.1371/journal.pone.0001510. PubMed DOI PMC
Sassi M., Lu Y., Zhang Y., Wang J., Dhonukshe P., Blilou I., Dai M., Li J., Gong X., Jaillais Y., et al. COP1 Mediates the Coordination of Root and Shoot Growth by Light through Modulation of PIN1- and PIN2-Dependent Auxin Transport in Arabidopsis. Development. 2012;139:3402–3412. doi: 10.1242/dev.078212. PubMed DOI
Dolan L., Duckett C.M., Grierson C., Linstead P., Schneider K., Lawson E., Dean C., Poethig S., Roberts K. Clonal Relationships and Cell Patterning in the Root Epidermis of Arabidopsis. Development. 1994;120:2465–2474.
Grierson C., Nielsen E., Ketelaarc T., Schiefelbein J. Root Hairs. Arab. Book/Am. Soc. Plant Biol. 2014;12:e0172. doi: 10.1199/tab.0172. PubMed DOI PMC
Salazar-Henao J.E., Schmidt W. An Inventory of Nutrient-Responsive Genes in Arabidopsis Root Hairs. Front. Plant Sci. 2016;7:237. doi: 10.3389/fpls.2016.00237. PubMed DOI PMC
Lee R.D.-W., Cho H.-T. Auxin, the Organizer of the Hormonal/Environmental Signals for Root Hair Growth. Front. Plant Sci. 2013;4:448. doi: 10.3389/fpls.2013.00448. PubMed DOI PMC
Park E., Nebenführ A. The Plant Cytoskeleton. Springer; New York, NY, USA: 2011. Cytoskeleton and Root Hair Growth. DOI
Grebe M., Friml J., Swarup R., Sandberg G., Terlou M., Palme K., Bennett M.J., Scheres B. Cell Polarity Signaling in Arabidopsis Involves a BFA-Sensitive Auxin Influx Pathway. Curr. Biol. 2002;12:329–334. doi: 10.1016/S0960-9822(02)00654-1. PubMed DOI
Grebe M. Ups of and Downs of Tissue and Planar Polarity in Plants. BioEssays. 2004;26:719–729. doi: 10.1002/bies.20065. PubMed DOI
Yokawa K., Fasano R., Kagenishi T., Baluška F. Light as Stress Factor to Plant Roots—Case of Root Halotropism. Front. Plant Sci. 2014;5:718. doi: 10.3389/fpls.2014.00718. PubMed DOI PMC
Mo M., Yokawa K., Wan Y., Baluska F. How and Why Do Root Apices Sense Light under the Soil Surface? Front. Plant Sci. 2015;6:775. doi: 10.3389/fpls.2015.00775. PubMed DOI PMC
Wan Y., Yokawa K., Baluška F. Arabidopsis Roots and Light: Complex Interactions. Mol. Plant. 2019;12:1428–1430. doi: 10.1016/j.molp.2019.10.001. PubMed DOI
Mishra B.S., Singh M., Aggrawal P., Laxmi A. Glucose and Auxin Signaling Interaction in Controlling Arabidopsis Thaliana Seedlings Root Growth and Development. PLoS ONE. 2009;4:e4502. doi: 10.1371/journal.pone.0004502. PubMed DOI PMC
Kircher S., Schopfer P. Photosynthetic Sucrose Acts as Cotyledon-Derived Long-Distance Signal to Control Root Growth during Early Seedling Development in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2012;109:11217–11221. doi: 10.1073/pnas.1203746109. PubMed DOI PMC
Leitner J., Petrášek J., Tomanov K., Retzer K., Pařezová M., Korbei B., Bachmair A., Zažímalová E., Luschnig C. Lysine63-Linked Ubiquitylation of PIN2 Auxin Carrier Protein Governs Hormonally Controlled Adaptation of Arabidopsis Root Growth. Proc. Natl. Acad. Sci. USA. 2012;109:8322–8327. doi: 10.1073/pnas.1200824109. PubMed DOI PMC
Singh A.P., Fridman Y., Friedlander-Shani L., Tarkowska D., Strnad M., Savaldi-Goldstein S. Activity of the Brassinosteroid Transcription Factors BRASSINAZOLE RESISTANT1 and BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1/BRASSINAZOLE RESISTANT2 Blocks Developmental Reprogramming in Response to Low Phosphate Availability. Plant Physiol. 2014;166:678–688. doi: 10.1104/pp.114.245019. PubMed DOI PMC
Billou I., Xu J., Wildwater M., Willemsen V., Paponov I., Frimi J., Heldstra R., Aida M., Palme K., Scheres B. The PIN Auxin Efflux Facilitator Network Controls Growth and Patterning in Arabidopsis Roots. Nature. 2005;433:39–44. doi: 10.1038/nature03184. PubMed DOI
Vieten A., Vanneste S., Wisniewska J., Benková E., Benjamins R., Beeckman T., Luschnig C., Friml J. Functional Redundancy of PIN Proteins Is Accompanied by Auxin-Dependent Cross-Regulation of PIN Expression. Development. 2005;132:4521–4531. doi: 10.1242/dev.02027. PubMed DOI
Nukarinen E., Ngele T., Pedrotti L., Wurzinger B., Mair A., Landgraf R., Börnke F., Hanson J., Teige M., Baena-Gonzalez E., et al. Quantitative Phosphoproteomics Reveals the Role of the AMPK Plant Ortholog SnRK1 as a Metabolic Master Regulator under Energy Deprivation. Sci. Rep. 2016;6:31697. doi: 10.1038/srep31697. PubMed DOI PMC
Menand B., Yi K., Jouannic S., Hoffmann L., Ryan E., Linstead P., Schaefer D.G., Dolan L. An Ancient Mechanism Controls the Development of Cells with a Rooting Function in Land Plants. Science. 2007;316:1477–1480. doi: 10.1126/science.1142618. PubMed DOI
Datta S., Prescott H., Dolan L. Intensity of a Pulse of RSL4 Transcription Factor Synthesis Determines Arabidopsis Root Hair Cell Size. Nat. Plants. 2015;1:1–6. doi: 10.1038/nplants.2015.138. PubMed DOI
Grabov A., Ashley M.K., Rigas S., Hatzopoulos P., Dolan L., Vicente-Agullo F. Morphometric Analysis of Root Shape. New Phytol. 2005;165:641–652. doi: 10.1111/j.1469-8137.2004.01258.x. PubMed DOI
Müller M., Schmidt W. Environmentally Induced Plasticity of Root Hair Development in Arabidopsis. Plant Physiol. 2004;134:409–419. doi: 10.1104/pp.103.029066. PubMed DOI PMC
Luschnig C., Gaxiola R.A., Grisafi P., Fink G.R. EIR1, a Root-Specific Protein Involved in Auxin Transport, Is Required for Gravitropism in Arabidopsis Thaliana. Genes Dev. 1998;12:2175–2187. doi: 10.1101/gad.12.14.2175. PubMed DOI PMC
Lessons Learned from the Studies of Roots Shaded from Direct Root Illumination