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
Grossniklaus U
中科院分区:
生物学1区
文献类型:
--
作者:
Boisson-Dernier A;Lituiev DS;Nestorova A;Franck CM;Thirugnanarajah S;Grossniklaus U

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花粉管生长非常迅速,以影响植物的受精作用。ANXUR受体样激酶通过H2O2和Ca2+信号将花粉管的细胞内生长机制与细胞外基质的状态联系起来,从而促进这种生长。越来越明显的是,植物中相当于细胞壁的细胞外基质(ECM)可以以远远超出其所谓的被动机械支持的方式影响细胞内活动。在植物中,生长的细胞使用感知细胞壁完整性的机制来协调细胞壁性能与内部生长机制,以避免生长停止或完整性丧失。这种协调是如何精确工作的尚不清楚。以前,我们报道,在尖端生长的花粉管的ANXUR受体样激酶(RLK)的CrRLK1L亚家族是必不可少的,以维持增长而不损失细胞壁的完整性在拟南芥。在这里,我们表明ANXUR RLK的过度表达通过过度激活胞吐作用和分泌的细胞壁物质的过度积累来抑制生长。此外,在两个部分冗余的花粉表达的NADPH氧化酶的突变的特性加上遗传相互作用的研究表明,ANXUR RLK的功能上游的NADPH氧化酶。使用H2O2敏感的Hyper和Ca2+敏感的YC3.60传感器在NADPH氧化酶缺陷的突变体,我们发现,NADPH氧化酶产生尖端本地化,脉动H2O2生产的功能,可能通过Ca2+通道激活,以保持稳定的尖端集中的Ca2+梯度在生长过程中。我们的研究结果支持一个模型,ECM传感受体调节活性氧的产生,Ca2+稳态,胞吐,以协调ECM性能与内部生长机制。尖端生长的细胞,如植物根毛和花粉管或真菌菌丝,其特征在于尖端集中的Ca2+梯度。这些尖端生长的细胞通过局部添加新的膜和细胞壁材料来紧密协调其细胞外基质(ECM)(植物细胞中的细胞壁)的松动和压力驱动的变形。在以惊人的速度生长以影响植物受精的花粉管中,一类称为ANXUR受体样激酶(RLK)的激酶感知细胞壁完整性的扰动,它们的丢失导致花粉管破裂。在这里,我们获得了新的见解细胞壁监视的机制,这些RLKs在模式植物拟南芥。我们发现,过表达ANXUR RLK过度激活胞吐作用,导致分泌的细胞壁物质过度积累,最终导致生长停滞。此外,我们发现ANXUR RLK在NADPH氧化酶的上游起作用,NADPH氧化酶是产生活性氧(ROS)的膜锚定酶。使用H2O2和Ca2+敏感的记者,我们表明,NADPH氧化酶产生尖端本地化的H2O2生产,这是需要保持一个稳定的,尖端集中的Ca2+梯度,这是至关重要的花粉管生长。我们假设ECM敏感受体,如ANXUR RLK,调节ROS产生,Ca2+稳态和胞吐作用,以协调ECM与细胞内部生长机制的状态。
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.
DOI: 10.1083/jcb.145.2.317
发表时间: 1999-04-19
影响因子: 7.8
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