Mechanism of Infection Thread Elongation in Root Hairs of Medicago truncatula and Dynamic Interplay with Associated Rhizobial Colonization

被引:138
作者
Fournier, Joelle [1 ]
Timmers, Antonius C. J. [1 ]
Sieberer, Bjoern J. [1 ]
Jauneau, Alain [2 ]
Chabaud, Mireille [1 ]
Barker, David G. [1 ]
机构
[1] INRA, CNRS, UMR 2594 441, Lab Interact Plantes Microorganismes, F-31320 Castanet Tolosan, France
[2] Inst Fed Rech 40, F-31326 Castanet Tolosan, France
关键词
D O I
10.1104/pp.108.125674
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
In temperate legumes, endosymbiotic nitrogen-fixing rhizobia gain access to inner root tissues via a specialized transcellular apoplastic compartment known as the infection thread (IT). To study IT development in living root hairs, a protocol has been established for Medicago truncatula that allows confocal microscopic observations of the intracellular dynamics associated with IT growth. Fluorescent labeling of both the IT envelope (AtPIP2;1-green fluorescent protein) and the host endoplasmic reticulum (green fluorescent protein-HDEL) has revealed that IT growth is a fundamentally discontinuous process and that the variable rate of root hair invagination is reflected in changes in the host cell cytoarchitecture. The concomitant use of fluorescently labeled Sinorhizobium meliloti has further revealed that a bacteria-free zone is frequently present at the growing tip of the IT, thus indicating that bacterial contact is not essential for thread progression. Finally, these in vivo studies have shown that gaps within the bacterial file are a common feature during the early stages of IT development, and that segments of the file are able to slide collectively down the thread. Taken together, these observations lead us to propose that (1) IT growth involves a host-driven cellular mechanism analogous to that described for intracellular infection by arbuscular mycorrhizal fungi; (2) the non-regular growth of the thread is a consequence of the rate-limiting colonization by the infecting rhizobia; and (3) bacterial colonization involves a combination of bacterial cell division and sliding movement within the extracellular matrix of the apoplastic compartment.
引用
收藏
页码:1985 / 1995
页数:11
相关论文
共 45 条
[1]   RHIZOBIUM-MELILOTI LIPOOLIGOSACCHARIDE NODULATION FACTORS - DIFFERENT STRUCTURAL REQUIREMENTS FOR BACTERIAL ENTRY INTO TARGET ROOT HAIR-CELLS AND INDUCTION OF PLANT SYMBIOTIC DEVELOPMENTAL RESPONSES [J].
ARDOUREL, M ;
DEMONT, N ;
DEBELLE, FD ;
MAILLET, F ;
DEBILLY, F ;
PROME, JC ;
DENARIE, J ;
TRUCHET, G .
PLANT CELL, 1994, 6 (10) :1357-1374
[2]   Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain [J].
Bhat, RA ;
Miklis, M ;
Schmelzer, E ;
Schulze-Lefert, P ;
Panstruga, R .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (08) :3135-3140
[3]   Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations [J].
Boisson-Dernier, A ;
Chabaud, M ;
Garcia, F ;
Bécard, G ;
Rosenberg, C ;
Barker, DG .
MOLECULAR PLANT-MICROBE INTERACTIONS, 2001, 14 (06) :695-700
[4]   Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression [J].
Boursiac, Y ;
Chen, S ;
Luu, DT ;
Sorieul, M ;
van den Dries, N ;
Maurel, C .
PLANT PHYSIOLOGY, 2005, 139 (02) :790-805
[5]   Plant cell wall remodelling in the rhizobium-legume symbiosis [J].
Brewin, NJ .
CRITICAL REVIEWS IN PLANT SCIENCES, 2004, 23 (04) :293-316
[6]   Four genes of Medicago truncatula controlling components of a nod factor transduction pathway [J].
Catoira, R ;
Galera, C ;
de Billy, F ;
Penmetsa, RV ;
Journet, EP ;
Maillet, F ;
Rosenberg, C ;
Cook, D ;
Gough, C ;
Dénarié, J .
PLANT CELL, 2000, 12 (09) :1647-1665
[7]   Efficient transformation of Medicago truncatula cv. Jemalong using the hypervirulent Agrobacterium tumefaciens strain AGL1 [J].
Chabaud, M ;
de Carvalho-Niebel, F ;
Barker, DG .
PLANT CELL REPORTS, 2003, 22 (01) :46-51
[8]   Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti [J].
Cheng, HP ;
Walker, GC .
JOURNAL OF BACTERIOLOGY, 1998, 180 (19) :5183-5191
[9]  
Dart PJ, 1974, BIOL NITROGEN FIXATI, P381
[10]   Nod factor perception during infection thread growth fine-tunes nodulation [J].
Den Herder, Jeroen ;
Vanhee, Celine ;
De Rycke, Riet ;
Corich, Viviana ;
Holsters, Marcelle ;
Goormachtig, Sofie .
MOLECULAR PLANT-MICROBE INTERACTIONS, 2007, 20 (02) :129-137