Abstract
Author SummaryTip-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.
Highlights
It is well established that growing animal cells control the biogenesis, deposition, and remodeling of their extracellular matrix (ECM)
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
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
Summary
It is well established that growing animal cells control the biogenesis, deposition, and remodeling of their extracellular matrix (ECM). Growing plant cells direct the deposition of the primary cell wall (CW): the plants rigid, carbohydrate-rich ECM that resists turgor pressure, yet is flexible enough to allow cell expansion. The cell must be kept informed about any environmental changes modifying the CW properties in order to avoid growth arrest or rupture. To circumvent these catastrophic scenarios, it has become increasingly evident that plant cells have developed mechanisms to sense CW integrity, which relay information about CW performance to the internal growth machinery. The molecular nature of this relay mechanism, remains largely unknown [3]
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