Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes

Abstract

Understanding how the cell uses a limited set of proteins to transduce very different signals into specific cellular responses is a central goal of cell biology and signal transduction disciplines. Although multifunctionality in signal transduction is widespread, the mechanisms that allow differential modes of signaling in multifunctional signaling pathways are not well defined. In legume plants, a common symbiosis signaling pathway composed of at least seven proteins mediates infection by both mycorrhizal fungi and rhizobial bacteria. Here we show that the symbiosis signaling pathway in legumes differentially transduces both bacterial and fungal signals (inputs) to generate alternative calcium responses (outputs). We show that these differential calcium responses are dependent on the same proteins, DMI1 and DMI2, for their activation, indicating an inherent flexibility in this signaling pathway. By using Lyapunov and other mathematical analyses, we discovered that both bacterial-induced and fungalinduced calcium responses are chaotic in nature. Chaotic systems require minimal energy to produce a wide spectrum of outputs in response to marginally different inputs. The flexibility provided by chaotic systems is consistent with the need to transduce two different signals, one from rhizobial bacteria and one from mycorrhizal fungi, by using common components of a single signaling pathway.chaos ͉ mycorrhization ͉ nodulation

The exudate from an arbuscular mycorrhizal fungus induces nitric oxide accumulation in Medicago truncatula roots

“…Most studies on early events in the AM interaction have used simplified experimental systems where the plant was physically separated from the fungus (Weidmann et al 2004;Kosuta et al 2008;Gutjahr et al 2009) or plant or fungal exudate was applied to the reciprocal symbiotic partner as a means of simulating the sudden appearance of diffusible signaling compounds (Buée et al 2000;Navazio et al 2007;Besserer et al 2006;Tamasloukht et al 2003;Chabaud et al 2011;Mukherjee and Ané 2011;Maillet et al 2011). In the present work, we followed the latter approach: a fungal exudate was obtained following the protocol that allowed Navazio et al (2007) to detect a transient rise of cytosolic Ca2+ in cultured soybean cells and Chabaud et al (2011) to highlight a nuclear Ca2+spiking in M. truncatula ROC.…”

“…DMI2 (for Doesn't Make Infection) is a leucine-rich repeat receptor-like kinase (Endre et al 2002), which is thought to transduce the perception of both rhizobial and AM fungal signals leading to the activation of DMI1, a putative cation channel localized at the nuclear envelope ). This cascade leads to prolonged oscillations of calcium concentration in the nucleus (Chabaud et al 2011) and perinuclear cytoplasm (Kosuta et al 2008). The calcium-and calmodulin-dependent protein kinase DMI3 ) acts downstream of the calcium spiking and is believed to decode the calcium signal, inducing the transcription of symbiosis-related genes (Oldroyd and Downie 2006), likely through the action of its substrate IPD3 (Interacting Protein of DMI3; Messinese et al 2007).…”

“…Recently, the upregulation of a membrane steroid-binding protein was also shown to be induced in epidermal/subepidermal cells in the vicinity of AM fungal hyphae (Kuhn et al 2010). Diffusible AM fungal signals were also shown to activate early events, such as changes in cytosolic (Navazio et al 2007;Kosuta et al 2008) and nuclear Ca2+ concentration (Chabaud et al 2011), and delayed processes, such as root branching (Oláh et al 2005) and starch accumulation in the root cortex (Gutjahr et al 2009). Recently, fungal exudates from Glomus intraradices were shown to contain a mixture of sulfated and nonsulfated lipochitooligosaccharides (LCO), which are responsible for the activation of MtENOD11 gene expression and the induction of lateral roots formation (Maillet et al 2011).…”

Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis

“…In analogy with nodules, where Ca2+ oscillations are considered the landmark of a successful interaction [28], Ca2+ has long been hypothesized to be involved in AMF signal transduction [29]. However, the first experimental evidence of Ca2+ as a transducer of mycorrhizal signals came from measurements of Ca2+ oscillations in M. truncatula root hairs in the presence of, but not in contact with AM hyphae [ 30]. The use of a nuclear cameleon probe has provided two additional crucial contributions: firstly, the nucleus is the main target of the signaling pathway; secondly, the nuclear location of Ca2+ oscillations is an indispensable step for the activation of the nuclear kinase DMI3 [ 24].…”

An STE12 gene identified in the mycorrhizal fungus Glomus intraradices restores infectivity of a hemibiotrophic plant pathogen

“…Whilst an extensive list of genes has been reported to be modulated within the established symbiosis (Balestrini & Lanfranco, 2006;Küster et al, 2007), few data are available about cellular and molecular events essential to fungal morphogenesis and root penetration during the early stages of AM interactions. Only a limited set of genes have been identified in plants which could be implicated in the perception of fungal signals necessary for the activation of signal transduction pathways (Kosuta et al, 2003(Kosuta et al, , 2008Weidmann et al, 2004; New Phytologist (2009) 181: [693][694][695][696][697][698][699][700][701][702][703][704][705][706][707] No claim to original French government works www.newphytologist.org…”