Dynamic Expression, Differential Regulation and Functional Diversity of the CNGC Family Genes in Cotton.

Junheng Zhao,Luole Liu,Hanfeng Zhang,Zengyuan Tian,Hongtu Cui,Haihong Shang,Tianming Li,Panyu Li,Song Peng,Ruqiang Xu

doi:10.3390/ijms23042041

Junheng Zhao, Luole Liu + Show 8 more

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https://doi.org/10.3390/ijms23042041

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Abstract

Cyclic nucleotide-gated channels (CNGCs) constitute a family of non-selective cation channels that are primarily permeable to Ca2+ and activated by the direct binding of cyclic nucleotides (i.e., cAMP and cGMP) to mediate cellular signaling, both in animals and plants. Until now, our understanding of CNGCs in cotton (Gossypium spp.) remains poorly addressed. In the present study, we have identified 40, 41, 20, 20, and 20 CNGC genes in G. hirsutum, G. barbadense, G. herbaceum, G. arboreum, and G. raimondii, respectively, and demonstrated characteristics of the phylogenetic relationships, gene structures, chromosomal localization, gene duplication, and synteny. Further investigation of CNGC genes in G. hirsutum, named GhCNGC1-40, indicated that they are not only extensively expressed in various tissues and at different developmental stages, but also display diverse expression patterns in response to hormones (abscisic acid, salicylic acid, methyl jasmonate, ethylene), abiotic (salt stress) and biotic (Verticillium dahlia infection) stimuli, which conform with a variety of cis-acting regulatory elements residing in the promoter regions; moreover, a set of GhCNGCs are responsive to cAMP signaling during cotton fiber development. Protein–protein interactions supported the functional aspects of GhCNGCs in plant growth, development, and stress responses. Accordingly, the silencing of the homoeologous gene pair GhCNGC1&18 and GhCNGC12&31 impaired plant growth and development; however, GhCNGC1&18-silenced plants enhanced Verticillium wilt resistance and salt tolerance, whereas GhCNGC12&31-silenced plants had opposite effects. Together, these results unveiled the dynamic expression, differential regulation, and functional diversity of the CNGC family genes in cotton. The present work has laid the foundation for further studies and the utilization of CNGCs in cotton genetic improvement.

Highlights

Introduction iationsCyclic nucleotide-gated channels (CNGCs) are nonselective cation channels first identified in animals; they form heterotetrameric complexes consisting of two or three different types of subunits, and are opened by the direct binding of cyclic nucleotides and modulated by Ca2+ /calmodulin and phosphorylation; their strong permeability for Ca2+ provides an intracellular Ca2+ signal that is crucially important for both excitation and adaptation, and for the channel’s function to mediate light adaptation and chemosensation, as well as playing roles in neuronal pathfinding or synaptic plasticity [1,2]
Given the notion that the rate of gene loss was higher in allotetraploid cotton [32,33], the CNGC family may be critical to cotton growth and development by retaining its size during evolution
20 CNGC genes in G. hirsutum, G. barbadense, G. herbaceum, G. arboreum, and G. raimondii, respectively. These genes are highly conserved during evolution across all the five cotton species above, and they are classified into five phylogenetic groups (I, II, III, IV-A and IV-B), conforming to the CNGC family in other plant species

Summary

Introduction

Cyclic nucleotide-gated channels (CNGCs) are nonselective cation channels first identified in animals; they form heterotetrameric complexes consisting of two or three different types of subunits, and are opened by the direct binding of cyclic nucleotides (cNMPs; cAMP and cGMP) and modulated by Ca2+ /calmodulin and phosphorylation; their strong permeability for Ca2+ provides an intracellular Ca2+ signal that is crucially important for both excitation and adaptation, and for the channel’s function to mediate light adaptation and chemosensation, as well as playing roles in neuronal pathfinding or synaptic plasticity [1,2]. Is an essential nutrient, and intracellular changes in free Ca2+ levels act as regulators in many growth and developmental processes and coordinate responses to developmental cues and environmental stimuli [5,6]; in contrast, recent advances support that cAMP (and cGMP) constitutes an important component of the complex signaling network, including key pathways mediated by hormones, lipid, sugar, Ca2+ , K+ , nitrate, etc. It is anticipated that CNGCs may play pivotal roles during growth and development in plants

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