Cellular plasticity and transcriptional reprogramming in plant-nematode interactions: insights into feeding site formation and plant defense

Abstract

Plant-parasitic nematodes, especially sedentary endoparasites, threaten global agriculture by inducing cellular plasticity in host plants to form specialized feeding structures. Sedentary nematodes such as root-knot and cyst nematodes establish feeding sites, including giant cells and syncytia, to extract nutrients from the host. Feeding site formation involves complex biological processes, including cell cycle activation, metabolic reprogramming, cytoskeleton rearrangement, and hormonal signaling. This review explores the underlying molecular mechanism driving plant cellular plasticity, focusing on the role of the transcription factors that regulate gene expression during organogenesis, peculiar to giant cells and syncytia, essential for the nematode's sustenance during the sedentary life stage. Key transcription factors, including members of the MYB, WRKY, ARF, ERF, and LBD families, are modulated by nematode effectors during compatible interactions to reprogram plant gene expression to facilitate the development of the nematode feeding site. Despite the roles of transcription factors in establishing feeding sites, they present other roles in regulating plant defense responses, thereby balancing growth reprogramming with the activation of plant immune signaling pathways. The review also highlights the allowance limit of plant physiological processes during cellular reprogramming and defense response, providing insights into how certain plants can resist nematode infection. Furthermore, emerging biotechnological strategies, including molecular breeding and gene editing, are discussed as potential approaches to disrupt nematode-induced reprogramming, highlighting novel avenues for enhancing crop resistance. Understanding the molecular mechanism and physiological dynamics between cellular plasticity and transcriptional regulation in plant-nematode interactions is essential for developing sustainable solutions to mitigate the impact of plant-parasitic nematodes on agricultural production.