Dataset Information

Immunoprofiling of Cell Wall Carbohydrate Modifications During Flooding-Induced Aerenchyma Formation in Fabaceae Roots.

ABSTRACT: 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.

SUBMITTER: Pegg T

PROVIDER: S-EPMC7008352 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Publications

Immunoprofiling of Cell Wall Carbohydrate Modifications During Flooding-Induced Aerenchyma Formation in Fabaceae Roots.

Pegg Timothy T Edelmann Richard R RR Gladish Daniel K DK

Frontiers in plant science 20200203

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 modi ...[more]

PMID: 32117353

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Project description:The longitudinal pattern of root aerenchyma formation of its relationship with the function of adventitious roots in rice remains unclear. In this study, the percentage of the aerenchyma area to the cross-sectional area (i.e., aerenchyma percentage) was fit with four non-linear models, namely, W0-Gompertz, Ti-Gompertz, logistic, and von Bertalanffy. Goodness-of-fit criteria such as the R 2, the Akaike information criterion (AIC), and the Bayesian information criterion (BIC) were used to select the model. The bias of the parameters was evaluated using the difference between the ordinary least squares-based parameter estimates and the mean of 1,000 bootstrap-based parameter estimates and the symmetry of the distributions of these parameters. The results showed that the Ti-Gompertz model, which had a high goodness-of-fit with an R 2 close to 1, lower AIC and BIC values, parameter estimates close to being unbiased, and good linear approximation, provided the best fit for the longitude pattern of rice aerenchyma formation with different root lengths among the competing models. Using the second- and third-order derivatives according to the distance from the root apex, the critical points of Ti-Gompertz were calculated. The rapid stage for aerenchyma formation was from the maximum acceleration point (1.38-1.76 cm from the root apex) to the maximum deceleration point (3.13-4.19 cm from the root apex). In this stage, the aerenchyma percentage increased by 5.3-15.7% per cm, suggesting that the cortical cells tended to die rapidly for the aerenchyma formation rather than for the respiration cost during this stage. Meanwhile, the volume of the aerenchyma of the entire roots could be computed using the integral function of the Ti-Gompertz model. We proposed that the longitudinal pattern of root aerenchyma formation modeled by the Ti-Gompertz model helped to deeply understand the relationship between the anatomical traits and physiological function in rice adventitious roots.

Project description:Background and aimsRice is one of the few crops able to withstand periods of partial or even complete submergence. One of the adaptive traits of rice is the constitutive presence and further development of aerenchyma which enables oxygen to be transported to submerged organs. The development of lysigenous aerenchyma is promoted by ethylene accumulating within the submerged plant tissues, although other signalling mechanisms may also co-exist. In this study, aerenchyma development was analysed in two rice (Oryza sativa) varieties, 'FR13A' and 'Arborio Precoce', which show opposite traits in flooding response in terms of internode elongation and survival.MethodsThe growth and survival of rice varieties under submergence was investigated in the leaf sheath of 'FR13A' and 'Arborio Precoce'. The possible involvement of ethylene and reactive oxygen species (ROS) was evaluated in relation to aerenchyma formation. Cell viability and DNA fragmentation were determined by FDA/FM4-64 staining and TUNEL assay, respectively. Ethylene production was monitored by gas chromatography and by analysing ACO gene expression. ROS production was measured by using Amplex Red assay kit and the fluorescent dye DCFH(2)-DA. The expression of APX1 was also evaluated. AVG and DPI solutions were used to test the effect of inhibiting ethylene biosynthesis and ROS production, respectively.Key resultsBoth the varieties displayed constitutive lysigenous aerenchyma formation, which was further enhanced when submerged. 'Arborio Precoce', which is characterized by fast elongation when submerged, showed active ethylene biosynthetic machinery associated with increased aerenchymatous areas. 'FR13A', which harbours the Sub1A gene that limits growth during oxygen deprivation, did not show any increase in ethylene production after submersion but still displayed increased aerenchyma. Hydrogen peroxide levels increased in 'FR13A' but not in 'Arborio Precoce'.ConclusionsWhile ethylene controls aerenchyma formation in the fast-elongating 'Arborio Precoce' variety, in 'FR13A' ROS accumulation plays an important role.

Dataset Information

Immunoprofiling of Cell Wall Carbohydrate Modifications During Flooding-Induced Aerenchyma Formation in Fabaceae Roots.

Publications

Immunoprofiling of Cell Wall Carbohydrate Modifications During Flooding-Induced Aerenchyma Formation in Fabaceae Roots.

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