ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases.
ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases.
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DOI:
10.1371/journal.pbio.1001719
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发表时间:
2013-11
期刊:
影响因子:
9.8
通讯作者:
Grossniklaus U
中科院分区:
文献类型:
--
作者:
Boisson-Dernier A;Lituiev DS;Nestorova A;Franck CM;Thirugnanarajah S;Grossniklaus U
Pollen tubes grow extremely rapidly to effect fertilization in plants. ANXUR receptor-like kinases facilitate this growth by linking the intracellular growth machinery of pollen tubes to the status of the extracellular matrix via H2O2 and Ca2+ signaling. It has become increasingly apparent that the extracellular matrix (ECM), which in plants corresponds to the cell wall, can influence intracellular activities in ways that go far beyond their supposedly passive mechanical support. In plants, growing cells use mechanisms sensing cell wall integrity to coordinate cell wall performance with the internal growth machinery to avoid growth cessation or loss of integrity. How this coordination precisely works is unknown. Previously, we reported that in the tip-growing pollen tube the ANXUR receptor-like kinases (RLKs) of the CrRLK1L subfamily are essential to sustain growth without loss of cell wall integrity in Arabidopsis. Here, we show that over-expression of the ANXUR RLKs inhibits growth by over-activating exocytosis and the over-accumulation of secreted cell wall material. Moreover, the characterization of mutations in two partially redundant pollen-expressed NADPH oxidases coupled with genetic interaction studies demonstrate that the ANXUR RLKs function upstream of these NADPH oxidases. Using the H2O2-sensitive HyPer and the Ca2+-sensitive YC3.60 sensors in NADPH oxidase-deficient mutants, we reveal that NADPH oxidases generate tip-localized, pulsating H2O2 production that functions, possibly through Ca2+ channel activation, to maintain a steady tip-focused Ca2+ gradient during growth. Our findings support a model where ECM-sensing receptors regulate reactive oxygen species production, Ca2+ homeostasis, and exocytosis to coordinate ECM-performance with the internal growth machinery. Tip-growing cells, such as plant root hairs and pollen tubes or fungal hyphae, are characterized by a tip-focused Ca2+ gradient. These tip-growing cells tightly coordinate the loosening and pressure-driven deformation of their extracellular matrix (ECM)—the cell wall in plant cells—by locally adding new membrane and cell wall materials. In pollen tubes, which grow at amazing speeds to effect fertilization in plants, a class of kinases called the ANXUR receptor-like kinases (RLKs) sense perturbations in cell wall integrity, and their loss leads to pollen tube rupture. Here, we gain new insights into the mechanism of cell wall surveillance by these RLKs in the model plant Arabidopsis. We show that over-expressing ANXUR RLKs over-activates exocytosis, causing an over-accumulation of secreted cell wall material that eventually leads to growth arrest. Moreover, we find that the ANXUR RLKs function upstream of NADPH oxidases, which are membrane-anchored enzymes that produce reactive oxygen species (ROS). Using H2O2- and Ca2+-sensitive reporters, we show that NADPH oxidases generate tip-localized H2O2 production, which is required to maintain a steady, tip-focused Ca2+ gradient that is essential for pollen tube growth. We postulate that ECM-sensing receptors, such as the ANXUR RLKs, regulate ROS production, Ca2+ homeostasis, and exocytosis to coordinate the status of the ECM with the cell's internal growth machinery.
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影响因子:
7.8
作者:
Kost, B;Lemichez, E;Spielhofer, P;Hong, Y;Tolias, K;Carpenter, C;Chua, N H
通讯作者:
Chua, N H
DOI:
10.1073/pnas.1005366107
发表时间:
2010-10-12
影响因子:
11.1
作者:
Duan, Qiaohong;Kita, Daniel;Wu, Hen-Ming
通讯作者:
Wu, Hen-Ming
DOI:
10.1111/j.1365-313x.2010.04190.x
发表时间:
2010-06-01
期刊:
The Plant journal : for cell and molecular biology
影响因子:
--
作者:
Costa A;Drago I;Behera S;Zottini M;Pizzo P;Schroeder JI;Pozzan T;Lo Schiavo F
通讯作者:
Lo Schiavo F
影响因子:
4.6
作者:
Boisson-Dernier, Aurelien;Roy, Sucharita;Grossniklaus, Ueli
通讯作者:
Grossniklaus, Ueli
影响因子:
11.6
作者:
Ischebeck, Till;Stenzel, Irene;Heilmann, Ingo
通讯作者:
Heilmann, Ingo