Literature DB >> 24927545

Plant roots use a patterning mechanism to position lateral root branches toward available water.

Yun Bao1, Pooja Aggarwal2, Neil E Robbins3, Craig J Sturrock4, Mark C Thompson4, Han Qi Tan2, Cliff Tham2, Lina Duan5, Pedro L Rodriguez6, Teva Vernoux7, Sacha J Mooney4, Malcolm J Bennett8, José R Dinneny9.   

Abstract

The architecture of the branched root system of plants is a major determinant of vigor. Water availability is known to impact root physiology and growth; however, the spatial scale at which this stimulus influences root architecture is poorly understood. Here we reveal that differences in the availability of water across the circumferential axis of the root create spatial cues that determine the position of lateral root branches. We show that roots of several plant species can distinguish between a wet surface and air environments and that this also impacts the patterning of root hairs, anthocyanins, and aerenchyma in a phenomenon we describe as hydropatterning. This environmental response is distinct from a touch response and requires available water to induce lateral roots along a contacted surface. X-ray microscale computed tomography and 3D reconstruction of soil-grown root systems demonstrate that such responses also occur under physiologically relevant conditions. Using early-stage lateral root markers, we show that hydropatterning acts before the initiation stage and likely determines the circumferential position at which lateral root founder cells are specified. Hydropatterning is independent of endogenous abscisic acid signaling, distinguishing it from a classic water-stress response. Higher water availability induces the biosynthesis and transport of the lateral root-inductive signal auxin through local regulation of tryptophan aminotransferase of Arabidopsis 1 and PIN-formed 3, both of which are necessary for normal hydropatterning. Our work suggests that water availability is sensed and interpreted at the suborgan level and locally patterns a wide variety of developmental processes in the root.

Entities:  

Keywords:  adaptive root response; auxin-regulated root patterning; moisture regulation; root development; root system architecture

Mesh:

Substances:

Year:  2014        PMID: 24927545      PMCID: PMC4078807          DOI: 10.1073/pnas.1400966111

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  29 in total

1.  Local, efflux-dependent auxin gradients as a common module for plant organ formation.

Authors:  Eva Benková; Marta Michniewicz; Michael Sauer; Thomas Teichmann; Daniela Seifertová; Gerd Jürgens; Jirí Friml
Journal:  Cell       Date:  2003-11-26       Impact factor: 41.582

2.  The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots.

Authors:  Ikram Blilou; Jian Xu; Marjolein Wildwater; Viola Willemsen; Ivan Paponov; Jirí Friml; Renze Heidstra; Mitsuhiro Aida; Klaus Palme; Ben Scheres
Journal:  Nature       Date:  2005-01-06       Impact factor: 49.962

Review 3.  Intrinsic and environmental response pathways that regulate root system architecture.

Authors:  J E Malamy
Journal:  Plant Cell Environ       Date:  2005-01       Impact factor: 7.228

Review 4.  To branch or not to branch: the role of pre-patterning in lateral root formation.

Authors:  Jaimie M Van Norman; Wei Xuan; Tom Beeckman; Philip N Benfey
Journal:  Development       Date:  2013-11       Impact factor: 6.868

5.  Changes in auxin response from mutations in an AUX/IAA gene.

Authors:  D Rouse; P Mackay; P Stirnberg; M Estelle; O Leyser
Journal:  Science       Date:  1998-02-27       Impact factor: 47.728

6.  An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis.

Authors:  Ive De Smet; Laurent Signora; Tom Beeckman; Dirk Inzé; Christine H Foyer; Hanma Zhang
Journal:  Plant J       Date:  2003-02       Impact factor: 6.417

7.  Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status.

Authors:  Paul E Verslues; Manu Agarwal; Surekha Katiyar-Agarwal; Jianhua Zhu; Jian-Kang Zhu
Journal:  Plant J       Date:  2006-02       Impact factor: 6.417

8.  Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis.

Authors:  Ive De Smet; Takuya Tetsumura; Bert De Rybel; Nicolas Frei dit Frey; Laurent Laplaze; Ilda Casimiro; Ranjan Swarup; Mirande Naudts; Steffen Vanneste; Dominique Audenaert; Dirk Inzé; Malcolm J Bennett; Tom Beeckman
Journal:  Development       Date:  2007-01-10       Impact factor: 6.868

9.  Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal.

Authors:  Ranjan Swarup; Eric M Kramer; Paula Perry; Kirsten Knox; H M Ottoline Leyser; Jim Haseloff; Gerrit T S Beemster; Rishikesh Bhalerao; Malcolm J Bennett
Journal:  Nat Cell Biol       Date:  2005-11       Impact factor: 28.824

Review 10.  Lateral root development in Arabidopsis: fifty shades of auxin.

Authors:  Julien Lavenus; Tatsuaki Goh; Ianto Roberts; Soazig Guyomarc'h; Mikaël Lucas; Ive De Smet; Hidehiro Fukaki; Tom Beeckman; Malcolm Bennett; Laurent Laplaze
Journal:  Trends Plant Sci       Date:  2013-05-20       Impact factor: 18.313

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  74 in total

Review 1.  Auxin response under osmotic stress.

Authors:  Victoria Naser; Eilon Shani
Journal:  Plant Mol Biol       Date:  2016-04-06       Impact factor: 4.076

Review 2.  Water transport, perception, and response in plants.

Authors:  Johannes Daniel Scharwies; José R Dinneny
Journal:  J Plant Res       Date:  2019-02-11       Impact factor: 2.629

Review 3.  Opportunities and challenges in the subsoil: pathways to deeper rooted crops.

Authors:  Jonathan P Lynch; Tobias Wojciechowski
Journal:  J Exp Bot       Date:  2015-01-11       Impact factor: 6.992

Review 4.  Hormone activities and the cell cycle machinery in immunity-triggered growth inhibition.

Authors:  M U Reitz; M L Gifford; P Schäfer
Journal:  J Exp Bot       Date:  2015-03-28       Impact factor: 6.992

5.  Evidence for root adaptation to a spatially discontinuous water availability in the absence of external water potential gradients.

Authors:  Kara R Lind; Oskar Siemianowski; Bin Yuan; Tom Sizmur; Hannah VanEvery; Souvik Banerjee; Ludovico Cademartiri
Journal:  Proc Natl Acad Sci U S A       Date:  2020-12-21       Impact factor: 11.205

6.  Periodic Lateral Root Priming: What Makes It Tick?

Authors:  Marta Laskowski; Kirsten H Ten Tusscher
Journal:  Plant Cell       Date:  2017-02-21       Impact factor: 11.277

7.  Variation in Adult Plant Phenotypes and Partitioning among Seed and Stem-Borne Roots across Brachypodium distachyon Accessions to Exploit in Breeding Cereals for Well-Watered and Drought Environments.

Authors:  Vincent Chochois; John P Vogel; Gregory J Rebetzke; Michelle Watt
Journal:  Plant Physiol       Date:  2015-05-14       Impact factor: 8.340

Review 8.  Beyond the barrier: communication in the root through the endodermis.

Authors:  Neil E Robbins; Charlotte Trontin; Lina Duan; José R Dinneny
Journal:  Plant Physiol       Date:  2014-08-14       Impact factor: 8.340

9.  Fine-tuning of root elongation by ethylene: a tool to study dynamic structure-function relationships between root architecture and nitrate absorption.

Authors:  Erwan Le Deunff; Julien Lecourt; Philippe Malagoli
Journal:  Ann Bot       Date:  2016-10-01       Impact factor: 4.357

Review 10.  Growing Out of Stress: The Role of Cell- and Organ-Scale Growth Control in Plant Water-Stress Responses.

Authors:  Wei Feng; Heike Lindner; Neil E Robbins; José R Dinneny
Journal:  Plant Cell       Date:  2016-08-08       Impact factor: 11.277

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