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OVERVIEW White, P. J. and Brown, P. H. Plant nutrition for sustainable development and global health 1073

Conn, S. and Gilliham, M. Comparative physiology of elemental distributions in plants


Miwa, K. and Fujiwara, T. Boron transport in plants: co-ordinated regulation of transporters 1103 Kobayashi, T., Ogo, Y., Aung, M. S., Nozoye, T., Itai, R. N., Nakanishi, H., Yamakawa, T. and Nishizawa, N. K. The spatial expression and regulation of transcription factors IDEF1 and IDEF2 1109 Eticha, D., Zahn, M., Bremer, M., Yang, Z., Rangel, A. F., Rao, I. M. and Horst, W. J. Transcriptomic analysis reveals differential gene expression in response to aluminium in common bean (Phaseolus vulgaris) genotypes 1119 Führs, H., Behrens, C., Gallien, S., Heintz, D., Van Dorsselaer, A., Braun, H.-P. and Horst, W. J. Physiological and proteomic characterization of manganese sensitivity and tolerance in rice (Oryza sativa) in comparison with barley (Hordeum vulgare) 1129

Couturier, J., Doidy, J., Guinet, F., Wipf, D., Blaudez, D. and Chalot, M. Glutamine, arginine and the amino acid transporter Pt-CAT11 play important roles during senescence in poplar 1159 Beatty, P. H., Anbessa, Y., Juskiw, P., Carroll, R. T., Wang, J. and Good, A. G. Nitrogen use efficiencies of spring barley grown under varying nitrogen conditions in the field and growth chamber 1171 Devau, N., Le Cadre, E., Hinsinger, P. and Gérard, F. A mechanistic model for understanding root-induced chemical changes controlling phosphorus availability 1183 White, P. J., Hammond, J. P., King, G. J., Bowen, H. C., Hayden, R. M., Meacham, M. C., Spracklen, W. P. and Broadley, M. R. Genetic analysis of potassium use efficiency in Brassica oleracea 1199

Contents continued on inside back cover

Pages 1073–1234 Volume 105 Number 7 June 2010

Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L. and Suzuki, A. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture 1141

Special Issue: Plant Nutrition


L IA E ion EC U trit SP ISS u tN an Pl



Volume 105 Number 7 June 2010


Volume 105 Number 7 June 2010

oxford issn 0305-7364 (Print) issn 1095-8290 (Online)



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ANNALS OF BOTANY An international journal founded in 1887 to publish on all aspects of the plant sciences, whether observational, experimental, theoretical or applied. The journal is managed by the Annals of Botany Company which is a Registered Charity, No. 237771: COMPANY MEMBERS

Contents from back cover Chatzav, M., Peleg, Z., Ozturk, L., Yazici, A., Fahima, T., Cakmak, I. and Saranga, Y. Genetic diversity for grain nutrients in wild emmer wheat: potential for wheat improvement 1211 Ding, G., Yang, M., Hu, Y., Liao, Y., Shi, L., Xu, F. and Meng, J. Quantitative trait loci affecting seed mineral concentrations in Brassica napus grown with contrasting phosphorus supplies 1221

Chairman H. G. Dickinson Vice-Chairman D. F. Cutler Secretary, Treasurer R. Hunt M. D. Bennett J. A. Bryant M. F. Fay C. Foyer J. S. Heslop-Harrison S. G. Hughes M. B. Jackson

Published monthly by Oxford University Press, Great Clarendon Street, Oxford OX2 6DP, UK

Notes for Authors The Annals of Botany accepts high quality papers from throughout the world, makes NO PAGE CHARGES, supplies free of charge a URL giving access to the PDF file and 25 OFFPRINTS of each paper published (additional copies may be ordered at the proof stage) and makes NO CHARGE FOR COLOUR PLATES. An exclusive licence in all papers accepted for publication must be assigned to the Annals of Botany Company, but the Company will not put any limitation on the personal freedom of the author to use material contained in the paper in other works of which he or she is the author.

Preparing and submitting manuscripts to the Annals of Botany A guide to submitting manuscripts to the Journal can be accessed from the Journal’s home page ( Please note that submission should normally be in electronic form. Contact details are: Annals of Botany Editorial Office, Department of Biology, University of Leicester, University Road, Leicester LE1 7RH, UK. E-mail:; Fax: +44 (0)116 2523330; Tel: +44 (0)116 2523396. © Annals of Botany Company 2010 All rights reserved; no part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise without prior written permission of the Publishers, or a licence permitting restricted copying issued in the UK by the Copyright Licensing Agency Ltd, 90 Tottenham Court Road, London W1P 9HE, or in the USA by the Copyright Clearance Center, 222 Rosewood Drive, Danvers, MA 01923. For those in the USA or Canada not registered with CCC, articles can be obtained by fax in 48 hours by calling: WISE for MedicineTM 1-800-667-WISE.

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Cover illustration: The inset photograph from the SCRI image collection shows barley grain ready for malting. Current research in plant mineral nutrition is addressing the sustainable production of food crops that contribute sufficient minerals for optimal animal and human nutrition. See White and Brown (pp. 1073–1080).

Disclaimer Statements of fact and opinion in the articles in Annals of Botany are those of the respective authors and contributors and not of Annals of Botany Company or Oxford University Press. Neither Oxford University Press nor Annals of Botany Company make any representation, express or implied, in respect of the accuracy of the material in this journal and cannot accept any legal responsibility or liability for any errors or omissions that may be made. The reader should make his/her own evaluation as to the appropriateness or otherwise of any experimental technique described. Typeset by Techset Composition Ltd, Salisbury, UK. Printed by C.O.S. Printers Pte Ltd, Singapore.

Chief Editor Professor J. S. (Pat) Heslop-Harrison Department of Biology, University of Leicester, University Road, Leicester LE1 7RH, UK. Tel/Fax: +44 (0)116 2523381/2523330.

Managing Editor: Dr David Frost Editorial Assistant: Alexandra Bunning Annals of Botany Editorial Office, Department of Biology, University of Leicester, University Road, Leicester LE1 7RH, UK. Tel/Fax: +44 (0)116 2523396/2523330. Papers for publication should be submitted electronically online as outlined in ‘Instructions to Authors’ available from the Journal’s homepage (

Regional Editors: Timothy D. Colmer, School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia. Tel/Fax: +61 (0)8 6488 1993/1108.

J. W. (Bill) Shipley, De´partement de Biologie, Universite´ de Sherbrooke, Sherbrooke, Quebec, Canada J1K 2R1. Tel/Fax: +1 819 821 8000/8049.

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Shao Jian Zheng, College of Life Science, Zhejiang University, Zijingang Campus, Hangzhou 310058, PR China. Tel/Fax: +86 571 88206438.

Special Category Editors: Stephen C. Fry, Botanical Briefings Editor. School of Tom L. Rost, Review Editor. Section (Department) of Plant Biological Sciences, University of Edinburgh, The King’s Biology, University of California, Davis, CA 95616, USA. Buildings, Edinburgh EH9 3JH, UK. Tel/Fax: +1 530 7520628/5410. Tel/Fax: +44 (0)131 6505320/6505392. Nigel Chaffey, News Editor. Bath Spa University, Bath, UK.

Editors Karine Alix. AgroParisTech, France.

David W. Lawlor. Rothamsted Research, Harpenden, UK.

John R. Barnett. University of Reading, UK.

Donald A. Levin. University of Texas, Austin, USA.

Susanne Barth. Teagasc, Oak Park, Ireland.

Jonathan P. Lynch. Penn State University, University Park, USA.

Anne K. Brysting. University of Oslo, Norway.

Alison A. Powell. University of Aberdeen, UK.

C. Alex Buerkle. University of Wyoming, USA.

Hilary Rogers. Cardiff University, UK.

Pamela K. Diggle. University of Colorado, Boulder, USA.

Margret Sauter. Christian-Albrechts-Universita¨t, Kiel, Germany.

Michael F. Fay.

Margaret Sedgley. University of New England, NSW, Australia.

Royal Botanic Gardens, Kew, UK.

Uwe G. Hacke. University of Alberta, Edmonton, Canada.

Elizabeth Sheffield. University of Manchester, UK.

Mick Hanley. University of Plymouth, UK.

Nick Smirnoff. University of Exeter, UK.

Simon J. Hiscock. University of Bristol, UK.

Jeannette Whitton. University of British Columbia, Vancouver, Canada.

International Review Board: July– December 2009 M. Aarts L. Adamec G. A˚gren J. A˚gren D. Albach T. Almeras M. Andrews E. Andrieu R. Angelini N. Anten A. Antmann A. Aparicio M. Archetti C. Arnold J. Arroyo H. Asard M. Ashikari H. Astrom C. Atkins B. Atwell D. Ayres A. Bu´rquez P. Baas S. Bai P. Balandier M.J. Banuelos Martinez E. Benavente J. Benitez D. Bergmann N. Bertin R. Bicknell C. Birch A. Bisio F.P.C. Blamey D.G. Blevins S. Bonser K. Boote M. Boudrie C.K. Boyce K. Bradford S. Brady D. Braun M. Broadley G. Brown J. Bruhl J. Brunet R. Buggs K. Burg M. Byrne Z. Cai A. Caicedo D. Cameron K. Cameron D. Campbell L. Campbell K.F. Cao B. Carlsward A. Carmo-Silva W. Chaloner C. Chan D. Charlesworth C. Chen J.-G. Chen D. Chittleborough N. Christodoulakis M.G. Chung Z. Chunqin J. Cooke D. Coomes L. Corelli-Grappadelli O. Coriton

J. Cornelis S. Crafts-Brandner J. Craine D. Crawford F. Crecente-Campo M. Cruzan I. Cuthill M. Damascos C. Damerval A. Davis A.J. Davy M. Daws P. De Reffye E. Delhaize L. Dennis K. Dexter M. Deyholos A. Diaz J. Dolezel R. Dolferus M. Dong J. Doyle J. Duckett D. Dudits S. Dudley D. Eamus A. Eckert A. Edlund L. Egerton Warburton D.B. Egli L. Ehrich E. Elle J. Ellis R. Ellis S. Emms P. Endress R. Ennos E. Epstein A. Escudero H. Ezura A. Faivre S.-Z Fei A. Fernie J. Fisher L. Fishman T. Fleming T. Flowers E.D. Ford M. Foster D. Frame G.G. Franchi M. Franco O. Franklin V.E. Franklin-Tong J. Freeland W. Friedman T. Fukao H. Funatsuki P.E. Garcia T. Garnett F. Gaymard X.-J. Ge B. Gehrke T. George O. Ghannoum P. Gibbs P. Goicoechea G. Goins I. Goldman C. Goodwillie E. Grabau

B. Gravendeel M. Grebe H. Greenway H. Griffiths M. Grusak M. Guerra F. Gugerli A. Gunawardena S. Guo V. Gutschick E. Ho¨randl J. Hall D. Hansen S. Hardegree S. Haviola M. Hawkesford M. Hedre´n B. Heinze A. Henry R. Henry I. Hensen A. Heredia S. Heredia A. Herrera M. Herrero J. Hibberd A. Higashitani D. Hincha T. Hirasawa T. Hirose J. Holland K. Holsinger O. Honnay J. Hormaza B. Husband I. Ibanez A. Igamberdiev A. Ishihara K. Ishizawa C. Ivey T. Izawa K. Jagadish R. Jansen C. Jeffree G. Jeronimidis S. Johnson F. Jones O. Junttila A. Karley L. Karlsson J. Karron E. Kazakou J. Keeley C. Kelleher C.P. Keller T. Kellogg D. Kemp R. Kesseli P. Kevan K. Kikuzawa L. Kinoshita K. Kitajima C. Klak E. Klein C. Knight P. Knox G. Koch M. Koch L. Kouwenberg D. Kubien H. Lu¨then

M. Lahaye A. Lang P.-E. Lauri C. Lavoie T. Lawson P. Lea E. Lebon R. Leimu F. Lens G. Leubner-Metzger C. Lexer Y.C. Liang H. Liao J. Liu T. Lowrey R. Lumaret E. Luschei A. Lux K. Lye J. Lynch J.F. Ma A. Makela T.T. Makino S. Maldonado D. Malinowski J. Maluszynska B. Mandak L. Marcelis A. Markkola N. Marron H. Martens J. Martin N. Martin H. Matsumoto G. Matthew S. Mayr A. McCormick M. McCully A. McKown H. Mebatsion H. Medrano M. Medrano H. Meimberg M. Mescher S. Meyer C. Micheneau B. Middleton J. Miguel Olano R. Milla N. Miller T. Miller R. Milne P. Minchin F. Minibayeva P. Minorsky Y. Miyazaki Y. Miyazawa M. Mogie A. Montesinos J. Moran D. Morgan K. Mueller K. Muller N. Murakami B. Murray M. Musci E. Nambara J. Nassar A. Neale D. Neale G. Neumann

N. Neves G. Noctor F. Normand N. Ohmido M. Olmstead M. Ono A. Ortiz E. Pacini S. Palacio C. Palma da Silva R. Papa J. Papenbrock C. Parisod O. Paun O. Pedersen C. Penel A. Penttinen G. Petersen C. Peterson M. Philipp A. Pieters M. Pirie K. Plassmann A. Polle L. Poorter G. Prenner R. Probert M. Proctor C. Proenc¸a J. Quero K. Raghothama R. Raguso N. Rajakaruna S. Ramachandran S. Razafimandimbison M. Reid R. Reid Z Rengel S. Renner D.-K. Ro E. Robbrecht J.J. Robledo-Arnuncio L. Rochefort L. Ronse de Craene T. Roose A. Rosati A. Roth-Nebelsick K. Roubelakis-Angelakis F. Rumsey P. Ryser M. Sakuta P. Saranpaa T. Sato S. Saura-Mas P. Schaberg K. Schierenbeck J. Schjoerring C. Schlo¨tterer P. Schlueter J. Schmidt E. Schranz A. Schubert S. Schubert L. Scott S. Shabala M. Sharma J. Shen S. Shimamura K.K. Shimizu H. Shou T. Silfver

R. Soreng D. Spooner D. Sprugel J. Sto¨cklin M. Stang A. Stephenson F. Sterck J.L. Stone G. Striker P. Struik S. Sugiyama M. Sussman G. Svensson J. Syvertsen R. Tahvonen S. Taketa C. Tang M. Taylor F.W. Telewski R. Testolin M. Thelander W.W. Thomas K. Thompson J. Thomson J. Thornley C. Thorogood I. Till-Bottraud H. Tobe H. Tsukaya W. Ulrich S. Unsicker V. Vadez F. Valladares M. Vallejo-Marin P. Van Bodegom R. Van de Berg M. Van Kleunen W. Van Riemsdijk C. Vance K. Vandepitte S. Vanderhoeven H. Vare A. Vegetti G. Vert R. Villar E. Visser J.M. Vivanco F. Volaire F. Wagner-Cremer K. Wang C. Wasternack B. Waters E. Waters W. Weckwerth A. Wetten P. White K.D. Whitney D. Williams J. Williams E. Woltering I. Woodward S.D. Wullschleger G. Xu T. Yamada J.L. Yang G. Yatskievych N. Yoccoz Q. Yu F.J. Zhao

Annals of Botany