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Autophagy promotes programmed cell death and corpse clearance in specific cell types of the Arabidopsis root cap.

ABSTRACT: Autophagy is a conserved quality control pathway that mediates the degradation of cellular components by targeting them to the lysosomes or vacuoles.¹ Autophagy has been implicated in the regulation of some regulated cell death processes in animal systems.² However, its function in developmentally controlled programmed cell death (dPCD) in plants remains little studied and controversial.³ Some studies have reported autophagy pro-survival roles,⁴^,⁵ while others have suggested pro-death functions for autophagy,⁶^,⁷ calling for further detailed investigations. Here, we investigated the role of autophagy in dPCD using the Arabidopsis root cap as an accessible and genetically tractable model system.⁸ In Arabidopsis, dPCD is an integral part of root cap differentiation, restricting root cap organ size to the root meristem.⁹ The root cap consists of two distinct tissues: the proximally positioned columella that is located at the very root tip and the lateral root cap (LRC) that flanks the root meristem up to its distal end at the start of the root elongation zone.¹⁰ We show that autophagic flux strongly increased prior to dPCD execution in both root cap tissues and depends on the key autophagy genes ATG2, ATG5, and ATG7. Systemic and organ-specific mutation of these genes shows delayed PCD execution and lack of postmortem corpse clearance in the columella but no defects in dPCD execution or corpse clearance in the distal LRC. Our results reveal a high degree of cell-type specificity in autophagy functions and suggest that autophagy roles in dPCD can considerably diverge between different cell types of the same plant organ.

SUBMITTER: Feng Q

PROVIDER: S-EPMC7612756 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Nitrogen-fixing heterocystous cyanobacteria are used as biofertilizer inoculants for stimulating plant growth but can also alleviate plant stress by exometabolite secretion. However, only a small number of studies have focused on elucidating the identity of said bioactives because of the wide array of exuded compounds. Here, we used the root hair assay (RHA) as a rapid programmed cell death (PCD) screening tool for characterizing the bioactivity of cyanobacteria Nostoc muscorum conditioned medium (CM) on Arabidopsis thaliana root hair stress tolerance. We found that heat-stressed A. thaliana pre-treated with N. muscorum CM fractions exhibited significantly lower root hair PCD levels compared to untreated seedlings. Treatment with CM increased stress tolerance by suppressing PCD in root hairs but not necrosis, indicating the bioactive compound was specifically modulating the PCD pathway and not a general stress response. Based on documented N. muscorum exometabolites, we identified the stress-responsive proline as a compound of interest and strong evidence from the ninhydrin assay and HPLC indicate that proline is present in N. muscorum CM. To establish whether proline was capable of suppressing PCD, we conducted proline supplementation experiments. Our results showed that exogenous proline had a similar effect on root hairs as N. muscorum CM treatment, with comparable PCD suppression levels and insignificant necrosis changes. To verify proline as one of the biologically active compounds in N. muscorum CM, we used three mutant A. thaliana lines with proline transporter mutations (lht1, aap1 and atprot1-1::atprot2-3::atprot3-2). Compared with the wild-type seedlings, PCD-suppression in lht1and aap1 mutants was significantly reduced when supplied with low proline (1-5 μM) levels. Similarly, pre-treatment with N. muscorum CM resulted in elevated PCD levels in all three mutant lines compared to wild-type seedlings. Our results show that plant uptake of cyanobacteria-derived proline alters their root hair PCD sensitivity threshold. This offers evidence of a novel biofertilizer mechanism for reducing stress-induced PCD levels, independent of the existing mechanisms documented in the literature.

Project description:Background and aimsDevelopment of the velamen radicum on the outer surface of the root epidermis is an important characteristic for water uptake and retention in some plant families, particularly epiphytic orchids, for survival under water-limited environments. Velamen radicum cells derive from the primary root meristem; however, following this development, velamen radicum cells die by incompletely understood processes of programmed cell death (PCD).MethodsWe combined the use of transmission electron microscopy, X-ray micro-tomography and transcriptome methods to characterize the major anatomical and molecular changes that occur during the development and death of velamen radicum cells of Cymbidium tracyanum, a typical epiphytic orchid, to determine how PCD occurs.Key resultsTypical changes of PCD in anatomy and gene expression were observed in the development of velamen radicum cells. During the initiation of PCD, we found that both cell and vacuole size increased, and several genes involved in brassinosteroid and ethylene pathways were upregulated. In the stage of secondary cell wall formation, significant anatomical changes included DNA degradation, cytoplasm thinning, organelle decrease, vacuole rupture and cell wall thickening. Changes were found in the expression of genes related to the biosynthesis of cellulose and lignin, which are instrumental in the formation of secondary cell walls, and are regulated by cytoskeleton-related factors and phenylalanine ammonia-lyase. In the final stage of PCD, cell autolysis was terminated from the outside to the inside of the velamen radicum. The regulation of genes related to autophagy, vacuolar processing enzyme, cysteine proteases and metacaspase was involved in the final execution of cell death and autolysis.ConclusionsOur results showed that the development of the root velamen radicum in an epiphytic orchid was controlled by the process of PCD, which included initiation of PCD, followed by formation of the secondary cell wall, and execution of autolysis following cell death.

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Autophagy promotes programmed cell death and corpse clearance in specific cell types of the Arabidopsis root cap.

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