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Cell wall hydrolases act in concert during aerenchyma development in sugarcane roots.

ABSTRACT: BACKGROUND AND AIMS:Cell wall disassembly occurs naturally in plants by the action of several glycosyl-hydrolases during different developmental processes such as lysigenous and constitutive aerenchyma formation in sugarcane roots. Wall degradation has been reported in aerenchyma development in different species, but little is known about the action of glycosyl-hydrolases in this process. METHODS:In this work, gene expression, protein levels and enzymatic activity of cell wall hydrolases were assessed. Since aerenchyma formation is constitutive in sugarcane roots, they were assessed in segments corresponding to the first 5 cm from the root tip where aerenchyma develops. KEY RESULTS:Our results indicate that the wall degradation starts with a partial attack on pectins (by acetyl esterases, endopolygalacturonases, ?-galactosidases and ?-arabinofuranosidases) followed by the action of ?-glucan-/callose-hydrolysing enzymes. At the same time, there are modifications in arabinoxylan (by ?-arabinofuranosidases), xyloglucan (by XTH), xyloglucan-cellulose interactions (by expansins) and partial hydrolysis of cellulose. Saccharification revealed that access to the cell wall varies among segments, consistent with an increase in recalcitrance and composite formation during aerenchyma development. CONCLUSION:Our findings corroborate the hypothesis that hydrolases are synchronically synthesized, leading to cell wall modifications that are modulated by the fine structure of cell wall polymers during aerenchyma formation in the cortex of sugarcane roots.

SUBMITTER: Grandis A

PROVIDER: S-EPMC6881219 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Cell wall hydrolases act in concert during aerenchyma development in sugarcane roots.

Grandis Adriana A Leite Débora C C DCC Tavares Eveline Q P EQP Arenque-Musa Bruna C BC Gaiarsa Jonas W JW Martins Marina C M MCM De Souza Amanda P AP Gomez Leonardo D LD Fabbri Claudia C Mattei Benedetta B Buckeridge Marcos S MS

Annals of botany 20191101 6

<h4>Background and aims</h4>Cell wall disassembly occurs naturally in plants by the action of several glycosyl-hydrolases during different developmental processes such as lysigenous and constitutive aerenchyma formation in sugarcane roots. Wall degradation has been reported in aerenchyma development in different species, but little is known about the action of glycosyl-hydrolases in this process.<h4>Methods</h4>In this work, gene expression, protein levels and enzymatic activity of cell wall hyd ...[more]

PMID: 31190078

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Project description:Understanding plant adaptation mechanisms to prolonged water immersion provides options for genetic modification of existing crops to create cultivars more tolerant of periodic flooding. An important advancement in understanding flooding adaptation would be to elucidate mechanisms, such as aerenchyma air-space formation induced by hypoxic conditions, consistent with prolonged immersion. Lysigenous aerenchyma formation occurs through programmed cell death (PCD), which may entail the chemical modification of polysaccharides in root tissue cell walls. We investigated if a relationship exists between modification of pectic polysaccharides through de-methyl esterification (DME) and the formation of root aerenchyma in select Fabaceae species. To test this hypothesis, we first characterized the progression of aerenchyma formation within the vascular stele of three different legumes-Pisum sativum, Cicer arietinum, and Phaseolus coccineus-through traditional light microscopy histological staining and scanning electron microscopy. We assessed alterations in stele morphology, cavity dimensions, and cell wall chemistry. Then we conducted an immunolabeling protocol to detect specific degrees of DME among species during a 48-hour flooding time series. Additionally, we performed an enzymatic pretreatment to remove select cell wall polymers prior to immunolabeling for DME pectins. We were able to determine that all species possessed similar aerenchyma formation mechanisms that begin with degradation of root vascular stele metaxylem cells. Immunolabeling results demonstrated DME occurs prior to aerenchyma formation and prepares vascular tissues for the beginning of cavity formation in flooded roots. Furthermore, enzymatic pretreatment demonstrated that removal of cellulose and select hemicellulosic carbohydrates unmasks additional antigen binding sites for DME pectin antibodies. These results suggest that additional carbohydrate modification may be required to permit DME and subsequent enzyme activity to form aerenchyma. By providing a greater understanding of cell wall pectin remodeling among legume species, we encourage further investigation into the mechanism of carbohydrate modifications during aerenchyma formation and possible avenues for flood-tolerance improvement of legume crops.

Dataset Information

Cell wall hydrolases act in concert during aerenchyma development in sugarcane roots.

Publications

Cell wall hydrolases act in concert during aerenchyma development in sugarcane roots.

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