Stress‐adaptive gene discovery by exploiting collective decision‐making of decentralized plant response systems

Abstract

Summary Despite having a network of cytoplasmic interconnections (plasmodesmata) facilitating rapid exchange of metabolites and signal molecules, plant cells use the extracellular matrix as an alternative route for cell–cell communication. The need for extracellular signalling in plasmodesmata‐networked tissues is baffling. A hypothesis is proposed that this phenomenon defines the plant extracellular matrix as a ‘democratic space’ for collective decision‐making in a decentralized system, similar to quorum‐sensing in bacteria. Extracellular communication enables signal integration and coordination across several cell layers through ligand‐activated plasma membrane receptors. Recent results from drought stress‐adaptive responses and light‐mediated signalling in cell death activation show operational utility of this decision‐making process. Opportunities are discussed for new innovations in drought gene discovery using platforms targeting the extracellular matrix.

Isolation of Arabidopsis extracellular ATP binding proteins by affinity proteomics and identification of PHOSPHOLIPASE C‐LIKE 1 as an extracellular protein essential for fumonisin B1 toxicity

“…Supporting the view that PLCL1 suppression is protective against FB1 toxicity is the observation that gene knockout mutants have considerable resistance to FB1 (Figure 6). Involvement in cell death of PLCL1, a protein in the mobile phase of the extracellular matrix, is consistent with the existence of secreted factors in growth media of Arabidopsis cell cultures known to seal the fate of cells to death when exposed to FB1 (Chivasa and Goodman, 2020).…”

“…In considering the fundamental question of why cells use a universal energy carrier as an extracellular signal (Chivasa, 2020), these studies indicate strong links between energy‐demanding processes (root growth and cell viability) to the apoplastic signalling ATP pool. The reason that external ATP is preferred over intracellular ATP as a signal in these processes is related to the hypothesis of collective decision making across several cell layers (Chivasa and Goodman, 2020), with PLCL1 emerging as a key protein in these processes.…”

Heat Stress Triggers Differential Protein Accumulation in the Extracellular Matrix of Sorghum Cell Suspension Cultures

“…Despite these efforts, our knowledge on contributions of the plant secretome to heat stress response is limited [58], yet such proteins participate in plant growth processes, cell signaling, and in response to unfavorable conditions [33][34][35]. Additionally, the plant apoplast is regarded as a functional space in which extracellular signaling systems are integrated and coordinated prior to responses being elicited [59].…”

Insights into Plant Extracellular ATP Signaling Revealed by the Discovery of an ATP-Regulated Transcription Factor

“…Firstly, the apoplast represents a compartment that may function to demarcate the extracellular signalling ATP pool from the intracellular energy pool. Secondly, the recent hypothesis that apoplast signalling represents a mechanism for collective decision-making in similar fashion to quorum-sensing bacteria identified eATP signalling as a classic example (Chivasa and Goodman, 2019). This study (Zhu et al, 2020) has now raised the possibility of the existence of additional receptor protein(s), which will certainly be subject to future research in addressing these fundamental questions.…”