Combined in Silico/in Vivo Analysis of Mechanisms Providing for Root Apical Meristem Self-organization and Maintenance

Overview

Journal Ann Bot

Publisher Oxford University Press

Specialty Biology

Date 2012 Apr 19

PMID 22510326

Citations 18

Authors

V V Mironova

N A Omelyanchuk

E S Novoselova

A V Doroshkov

F V Kazantsev

A V Kochetov

N A Kolchanov

E Mjolsness

V A Likhoshvai

Affiliations

Soon will be listed here.

Abstract

Background And Aims: The root apical meristem (RAM) is the plant stem cell niche which provides for the formation and continuous development of the root. Auxin is the main regulator of RAM functioning, and auxin maxima coincide with the sites of RAM initiation and maintenance. Auxin gradients are formed due to local auxin biosynthesis and polar auxin transport. The PIN family of auxin transporters plays a critical role in polar auxin transport, and two mechanisms of auxin maximum formation in the RAM based on PIN-mediated auxin transport have been proposed to date: the reverse fountain and the reflected flow mechanisms.

Methods: The two mechanisms are combined here in in silico studies of auxin distribution in intact roots and roots cut into two pieces in the proximal meristem region. In parallel, corresponding experiments were performed in vivo using DR5::GFP Arabidopsis plants.

Key Results: The reverse fountain and the reflected flow mechanism naturally cooperate for RAM patterning and maintenance in intact root. Regeneration of the RAM in decapitated roots is provided by the reflected flow mechanism. In the excised root tips local auxin biosynthesis either alone or in cooperation with the reverse fountain enables RAM maintenance.

Conclusions: The efficiency of a dual-mechanism model in guiding biological experiments on RAM regeneration and maintenance is demonstrated. The model also allows estimation of the concentrations of auxin and PINs in root cells during development and under various treatments. The dual-mechanism model proposed here can be a powerful tool for the study of several different aspects of auxin function in root.

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References

Ulmasov T, Murfett J, Hagen G, Guilfoyle T . Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell. 1997; 9(11):1963-71. PMC: 157050. DOI: 10.1105/tpc.9.11.1963. View

Swarup R, Kramer E, Perry P, Knox K, Leyser H, Haseloff J . Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat Cell Biol. 2005; 7(11):1057-65. DOI: 10.1038/ncb1316. View

Wisniewska J, Xu J, Seifertova D, Brewer P, Ruzicka K, Blilou I . Polar PIN localization directs auxin flow in plants. Science. 2006; 312(5775):883. DOI: 10.1126/science.1121356. View

Jonsson H, Heisler M, Shapiro B, Meyerowitz E, Mjolsness E . An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci U S A. 2006; 103(5):1633-8. PMC: 1326488. DOI: 10.1073/pnas.0509839103. View

Scacchi E, Salinas P, Gujas B, Santuari L, Krogan N, Ragni L . Spatio-temporal sequence of cross-regulatory events in root meristem growth. Proc Natl Acad Sci U S A. 2010; 107(52):22734-9. PMC: 3012524. DOI: 10.1073/pnas.1014716108. View

Wabnik K, Kleine-Vehn J, Balla J, Sauer M, Naramoto S, Reinohl V . Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol Syst Biol. 2010; 6:447. PMC: 3018162. DOI: 10.1038/msb.2010.103. View

Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J . An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell. 1999; 99(5):463-72. DOI: 10.1016/s0092-8674(00)81535-4. View

Jiang K, Feldman L . Regulation of root apical meristem development. Annu Rev Cell Dev Biol. 2005; 21:485-509. DOI: 10.1146/annurev.cellbio.21.122303.114753. View

Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V, Friml J . Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev. 2006; 20(20):2902-11. PMC: 1619939. DOI: 10.1101/gad.390806. View

10.

Feugier F, Iwasa Y . How canalization can make loops: a new model of reticulated leaf vascular pattern formation. J Theor Biol. 2006; 243(2):235-44. DOI: 10.1016/j.jtbi.2006.05.022. View

11.

Zazimalova E, Murphy A, Yang H, Hoyerova K, Hosek P . Auxin transporters--why so many?. Cold Spring Harb Perspect Biol. 2010; 2(3):a001552. PMC: 2829953. DOI: 10.1101/cshperspect.a001552. View

12.

Petersson S, Johansson A, Kowalczyk M, Makoveychuk A, Wang J, Moritz T . An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell. 2009; 21(6):1659-68. PMC: 2714926. DOI: 10.1105/tpc.109.066480. View

13.

Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J . The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature. 2005; 433(7021):39-44. DOI: 10.1038/nature03184. View

14.

Woodward A, Bartel B . Auxin: regulation, action, and interaction. Ann Bot. 2005; 95(5):707-35. PMC: 4246732. DOI: 10.1093/aob/mci083. View

15.

Benkova E, Ivanchenko M, Friml J, Shishkova S, Dubrovsky J . A morphogenetic trigger: is there an emerging concept in plant developmental biology?. Trends Plant Sci. 2009; 14(4):189-93. DOI: 10.1016/j.tplants.2009.01.006. View

16.

Likhoshvai V, Omelianchuk N, Mironova V, Fadeev S, Melsness E, Kolchanov N . [Mathematical model of auxin distribution in the plant root]. Ontogenez. 2008; 38(6):446-56. View

17.

Vieten A, Vanneste S, Wisniewska J, Benkova E, Benjamins R, Beeckman T . Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development. 2005; 132(20):4521-31. DOI: 10.1242/dev.02027. View

18.

Ljung K, Hull A, Kowalczyk M, Marchant A, Celenza J, Cohen J . Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol. 2002; 49(3-4):249-72. View

19.

Ikeda Y, Men S, Fischer U, Stepanova A, Alonso J, Ljung K . Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat Cell Biol. 2009; 11(6):731-8. DOI: 10.1038/ncb1879. View

20.

Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof Y, Kleine-Vehn J . Auxin inhibits endocytosis and promotes its own efflux from cells. Nature. 2005; 435(7046):1251-6. DOI: 10.1038/nature03633. View