An ORGANELLAR EXONUCLEASE is essential for nitric oxide dependent pollen tube growth responses

Nitric oxide (NO) is a universal and ancient signaling molecule that modulates a myriad of biological processes in various organisms. In animals, NO interacts with and activates the guanylate cyclase at an allosteric heme-binding site, causing an elevation of the second messenger cGMP, resulting in vasodilation. In plants, this heme-based sensing of NO appears to be elusive despite NO being associated with broad plant processes including the growth, re-orientation and ovule targeting of pollen tubes. Here, we report the identification of an ORGANELLAR EXONUCLEASE, OEX1, as a novel hemoprotein, and show that pollen tubes of oex1 mutant plants have markedly reduced sensitivity to NO. Spectroscopic data show that OEX1 generates Soret peak diagnostic of heme interaction, which can be oxidized, reduced and NO-ligated accordingly. Importantly, substitution of key amino acids at the heme-interacting site lowers the Soret signatures indicating reduced heme and concomitantly also NO interactions. Furthermore, comparative genomics reveals NO-dependent molecular functions and biological processes that are affected by OEX1 thereby linking heme-sensing of NO to responses at the systems level. As a fast-diffusible gaseous signaling molecule, the molecular perception is crucial for the maintenance of cellular homeostasis under changing environmental conditions, thus the extension of heme-based gas sensing studies to crops could enhance the effectiveness of NO application in horticulture.