Page:Cell-to-Cell Communication During Plant-Pathogen Interaction.pdf/1

MPMI Vol. 35, No. 2, 2022, pp. 98–108, https://doi.org/10.1094/MPMI-09-21-0221-CR CURRENT REVIEW

Naheed Tabassum and Ikram Blilou King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia Accepted 11 October 2021.

''Being sessile, plants are continuously challenged by changes in their surrounding environment and must survive and defend themselves against a multitude of pathogens. Plants have evolved a mode for pathogen recognition that activates signaling cascades such as reactive oxygen species, mitogenactivated protein kinase, and Ca pathways, in coordination with hormone signaling, to execute the defense response at the local and systemic levels. Phytopathogens have evolved to manipulate cellular and hormonal signaling and exploit hosts’ cell-to-cell connections in many ways at multiple levels. Overall, triumph over pathogens depends on how efficiently the pathogens are recognized and how rapidly the plant response is initiated through efficient intercellular communication via apoplastic and symplastic routes. Here, we review how intercellular communication in plants is mediated, manipulated, and maneuvered during plant-pathogen interaction.''

Keywords: bacterial pathogenesis, cell-to-cell communication, fungus–plant interactions, nematode–plant interactions, oomycete– plant interactions, plant defense, plant responses to pathogens, plasmodesmata, phytohormone, virus movement, virus–plant interactions

Plants are constantly challenged by their continuously changing environment and are hijacked by a myriad of soil and airborne pathogens. To thrive in these unstable conditions, plants have evolved an excellent cell-to-cell communication system. In both plants and animals, cell-to-cell communication is a process that is highly regulated. Cells must receive the proper information required for specifying cell fate, forming tissues and organs, and building a robust defense mechanism against pathogens. Here, we highlight how intercellular communication is mediated in plants and how pathogens take advantage of this system to dupe plants by exploiting their two main types of communication: apoplastic and symplastic.

Apoplastic communication. The apoplast is the space outside the plasma membrane (PM), within which water and solutes can be freely transported across tissues or organs. Therefore, the apoplast is an ideal site for propagating and spreading pathogens from cell to cell. However, plants tightly regulate the essential apoplastic content targeted by the pathogens such as water, sugar, iron, reactive oxygen species (ROS), and pH in response to an attack (Aung et al. 2018; Qi et al. 2017). Plants also create apoplastic barriers by remodeling their cell membranes and walls in response to pathogens to restrict an infection.

A recent study revealed that the apoplast mediates the transport of such hormones as salicylic acid (SA) during pathogen infection in leaves. The accumulation of SA in an apoplast is driven by a pH gradient and is regulated by the cuticle (Lim et al. 2020). One of the critical apoplastic communication methods is long-distance ROS signaling during the respiratory or oxidative burst in response to abiotic or biotic stimuli. Nicotinamide adenine dinucleotide phosphate oxidase (NADPH oxidase), a PM-localized enzyme, produces superoxide radicals in the apoplast, which are converted to H2O2 either spontaneously or by superoxide dismutase present in the apoplast. However, apoplastic communication can be obstructed by apoplastic salt precipitates (Ranathunge et al. 2005).

Symplastic communication. To overcome a rigid cell wall, plants have evolved symplastic communication through pores connecting cytoplasmic streams of two adjacent cells. Traversing the cell wall, plasmodesmata (PDs) are intercellular pores or bridges that allow symplastic communication between adjacent cells. PDs facilitate intercellular trafﬁcking, passage, and signaling between cells (Lucas and Lee 2004). Structurally, they are lined by the PM and occupied by an intricate and complex structure of the endoplasmic reticulum (ER) fueled with PD and cytoskeletal proteins such as actin and myosin. The cylindrical segment of ER connecting two cells is known as a desmotubule. The lipid and protein composition of the PD PM is different from the rest of the cellular PM, which functions as a discrete PM microdomain (Fernandez-Calvino et al. 2011; Grison et al. 2015). Transmission electron microscopy shows a typical (simple) PD with a diameter of 50 nM (Bell and Oparka 2011).

In addition to nutrients, hormones, signaling molecules, and RNA, the PDs actively facilitate the trafﬁcking of numerous noncell-autonomous proteins in different plant organs (Gundu et al. 2020). In the shoot apical meristem, the homeodomain transcription factor WUSCHEL (WUS) is expressed in the organizing center, and its protein moves to the stem cells located at the outermost cell layer through the PD to keep them in an undifferentiated state and, thus, function noncell-autonomously (Daum et al. 2014). In roots, the cell-fate determinant SHORTROOT (SHR) moves from the stele to the outer layer, which is the endodermis and quiescent center, to control asymmetric cell division that gives rise to the cortex and endodermis to promote the The author(s) declare no conﬂict of interest.

The author(s) have dedicated the work to the public domain under the Creative Commons CC0 “No Rights Reserved” license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2022.

98 / Molecular Plant-Microbe Interactions