Aerenchyma Formation In Adventitious Roots Research Articles

Unravelling the role of adventitious roots under priming-induced tolerance to waterlogging stress in wheat

Waterlogging is a significant environmental stressor that can have detrimental effects on crop yields. Waterlogging priming has emerged as a promising technique for enhancing plant waterlogging tolerance. However, the underlying mechanisms behind the regulation of root resistance, particularly adventitious roots (ARs), in wheat under waterlogging stress remain unclear. In this study, we subjected plants to waterlogging priming for two days at the two-leaf stage, followed by seven days of waterlogging stress after a ten-day recovery period to investigate the morphological and anatomical structure and physiological functions of ARs in wheat. Our results demonstrated that primed plants under waterlogging stress (PW) had increased numbers of ARs, improved gas exchange, and enhanced aerenchyma formation in ARs, leading to normal plant respiration when compared to non-primed plants under waterlogging stress treatment (CW). PW up-regulated the expression of cell wall remodeling genes (CEL, XET), reactive oxygen species (ROS) production-related gene (RBOH1), and ethylene biosynthesis-related genes (ACS2, ACS4) in ARs, and increased anaerobic respiratory enzyme activity, thus preserving the supply of soluble sugars in ARs and providing more materials and energy for adventitious root regeneration compared to CW. Overall, waterlogging priming improved the waterlogging tolerance of both above-ground and ARs in wheat, reducing the severity of damage caused by waterlogging. Our findings provide new insights into the mechanisms underlying waterlogging priming and suggest that it may be a promising strategy for mitigating the adverse effects of waterlogging on crop productivity.

Aerenchyma Formation in Adventitious Roots of Tall Fescue and Cocksfoot under Waterlogged Conditions

The formation of aerenchyma in adventitious roots is one of the most crucial adaptive traits for waterlogging tolerance in plants. Pasture grasses, like other crops, can be affected by waterlogging, and there is scope to improve tolerance through breeding. In this study, two summer-active cocksfoot (Dactylis glomerata L.) cultivars, Lazuly and Porto, and two summer-active tall fescue (Lolium arundinaceum Schreb., syn. Festuca arundinacea Schreb.) cultivars, Hummer and Quantum II MaxP, were selected to investigate the effects of waterlogging on root growth and morphological change. Cultivars were subjected to four periods of waterlogging treatments (7, 14, 21 and 28 days), while comparable plants were kept under free drained control conditions. The experiment was arranged as a split–split plot design, with waterlogging treatments (waterlogged, control) considered as main plots, time periods (days of waterlogging) as subplots and cultivars as sub-subplots. Plants began to show signs of waterlogging stress 14–21 days after the onset of waterlogging treatments. There were no significant differences in shoot biomass between the waterlogged and control plants of any cultivar. However, waterlogging significantly reduced root dry matter in all cultivars, with greater reduction in cocksfoot (56%) than in tall fescue (38%). Waterlogging also led to increased adventitious root and aerenchyma formation in both species. Cocksfoot cultivars showed a greater increase in adventitious roots, while tall fescue cultivars had a greater proportion of aerenchyma. Both cultivars within each species showed similar responses to waterlogging treatments. However, an extended screening program is needed to identify whether there are varietal differences within species, which could be used to discover genes related to aerenchyma or adventitious root formation (waterlogging tolerance) for use in breeding programs.

Histological Observation of Primary and Secondary Aerenchyma Formation in Adventitious Roots of Syzygium kunstleri (King) Bahadur and R.C.Gaur Grown in Hypoxic Medium

Trees growing in wetlands develop adventitious roots from the trunk during the rainy season and adapt to the flooded environment by forming primary (schizogenous or lysigenous) and secondary aerenchyma in the roots. Therefore, it is necessary to clarify the formation process of each type of aerenchyma in these adventitious roots. In this study, saplings of Syzygium kunstleri (King) Bahadur and R.C.Gaur were grown under four different treatments, and a total of 12 adventitious roots generated from trunks were used to clarify the distribution of each aerenchyma type in the roots using light or epi-florescence microscopy. Schizogenous aerenchyma was observed in the root tips where the root color was white or light brown, whereas lysigenous aerenchyma was found at some distance from the root tip where the root color gradually changed from light to dark brown. The secondary aerenchyma and periderm were observed in dark brown parts near the root base. None or only one layer of phellem cells was detected in the white roots near the root tip, but dark brown roots near the root base had at least three layers of phellem cells. Considering these results, oxygen transportation may occur between primary and secondary aerenchyma at the point where two or more layers of phellem cells are formed.

Waterlogging of Winter Crops at Early and Late Stages: Impacts on Leaf Physiology, Growth and Yield.

Waterlogging is expected to increase as a consequence of global climate change, constraining crop production in various parts of the world. This study assessed tolerance to 14-days of early- or late-stage waterlogging of the major winter crops wheat, barley, rapeseed and field pea. Aerenchyma formation in adventitious roots, leaf physiological parameters (net photosynthesis, stomatal and mesophyll conductances, chlorophyll fluorescence), shoot and root growth during and after waterlogging, and seed production were evaluated. Wheat produced adventitious roots with 20–22% of aerenchyma, photosynthesis was maintained during waterlogging, and seed production was 86 and 71% of controls for early- and late-waterlogging events. In barley and rapeseed, plants were less affected by early- than by late-waterlogging. Barley adventitious roots contained 19% aerenchyma, whereas rapeseed did not form aerenchyma. In barley, photosynthesis was reduced during early-waterlogging mainly by stomatal limitations, and by non-stomatal constraints (lower mesophyll conductance and damage to photosynthetic apparatus as revealed by chlorophyll fluorescence) during late-waterlogging. In rapeseed, photosynthesis was mostly reduced by non-stomatal limitations during early- and late-waterlogging, which also impacted shoot and root growth. Early-waterlogged plants of both barley and rapeseed were able to recover in growth upon drainage, and seed production reached ca. 79–85% of the controls, while late-waterlogged plants only attained 26–32% in seed production. Field pea showed no ability to develop root aerenchyma when waterlogged, and its photosynthesis (and stomatal and mesophyll conductances) was rapidly decreased by the stress. Consequently, waterlogging drastically reduced field pea seed production to 6% of controls both at early- and late-stages with plants being unable to resume growth upon drainage. In conclusion, wheat generates a set of adaptive responses to withstand 14 days of waterlogging, barley and rapeseed can still produce significant yield if transiently waterlogged during early plant stages but are more adversely impacted at the late stage, and field pea is not suitable for areas prone to waterlogging events of 14 days at either growth stage.

Ethylene-dependent aerenchyma formation in adventitious roots is regulated differently in rice and maize.

In roots of gramineous plants, lysigenous aerenchyma is created by the death and lysis of cortical cells. Rice (Oryza sativa) constitutively forms aerenchyma under aerobic conditions, and its formation is further induced under oxygen-deficient conditions. However, maize (Zea mays) develops aerenchyma only under oxygen-deficient conditions. Ethylene is involved in lysigenous aerenchyma formation. Here, we investigated how ethylene-dependent aerenchyma formation is differently regulated between rice and maize. For this purpose, in rice, we used the reduced culm number1 (rcn1) mutant, in which ethylene biosynthesis is suppressed. Ethylene is converted from 1-aminocyclopropane-1-carboxylic acid (ACC) by the action of ACC oxidase (ACO). We found that OsACO5 was highly expressed in the wild type, but not in rcn1, under aerobic conditions, suggesting that OsACO5 contributes to aerenchyma formation in aerated rice roots. By contrast, the ACO genes in maize roots were weakly expressed under aerobic conditions, and thus ACC treatment did not effectively induce ethylene production or aerenchyma formation, unlike in rice. Aerenchyma formation in rice roots after the initiation of oxygen-deficient conditions was faster and greater than that in maize. These results suggest that the difference in aerenchyma formation in rice and maize is due to their different mechanisms for regulating ethylene biosynthesis.

Waterlogging tolerance in barley is associated with faster aerenchyma formation in adventitious roots

Plant adaptation to waterlogged conditions requires a set of morphological and physiological/biochemical changes. The formation of aerenchyma is one of the most crucial adaptive traits for waterlogging tolerance. Enzymatic scavenging may also potentially contribute to waterlogging tolerance by providing detoxification of reactive oxygen species (ROS). Changes of root porosity (as an indicator of aerenchyma formation) and activities in leaves of four major antioxidant enzymes, γ-amino butyric acid (GABA) and lactic acid contents in roots were evaluated in six barley genotypes contrasting in waterlogging tolerance. Soil waterlogging caused significant increases in adventitious root porosity in all genotypes. Waterlogging-tolerant genotypes showed not only significantly higher adventitious root porosity than sensitive genotypes but also much faster development of aerenchyma. The greatest difference in adventitious root porosity among genotypes was observed after 7 days of waterlogging treatment. At the same time, antioxidant enzyme activities in leaves, GABA and lactic acid contents in roots did not correlate with waterlogging tolerance. A faster formation of aerenchyma in adventitious roots is one of the key factors for waterlogging tolerance in barley. This protocol is recommended to be applied in future studies to identify molecular markers linked to this trait using appropriate mapping populations.

Screening of candidate genes associated with constitutive aerenchyma formation in adventitious roots of the teosinte Zea nicaraguensis

Zea nicaraguensis (teosinte), a wild relative of maize (Zea mays ssp. mays), constitutively forms aerenchyma, which contributes to plant waterlogging tolerance, in the root cortex in drained soil, whereas maize (inbred line Mi29) does not. One with highest logarithm of odds (LOD) among quantitative trait loci (QTLs) that control constitutive aerenchyma formation in Z. nicaraguensis is Qaer1.05-6 on chromosome 1. Here, we attempted to identify genes in Qaer1.05-6 by comparing cDNA libraries from Mi29, Z. nicaraguensis and a hybrid (BC4F1 #62) carrying Qaer1.05-6. We first confirmed that constitutive aerenchyma formation was apparently observed in the order Z. nicaraguensis > BC4F1 #62 > Mi29. Contigs were assembled from cDNAs pooled from the three lines. We identified 1,868 contigs in the region on chromosome 1 that contained Qaer1.05-6. These contigs were screened for contigs that were predominantly composed of cDNAs from BC4F1 #62 and Z. nicaraguensis (no more than 10% of cDNAs from Mi29). Twenty-one such contigs were found and the genes they encoded were identified. In a real-time reverse transcription-polymerase chain reaction (RT- PCR) analysis, expression of six of these genes in BC4F1 #62 was at least double that in Mi29, making them candidates for genes associated with constitutive aerenchyma formation.

Diversity in root aeration traits associated with waterlogging tolerance in the genus Hordeum

Growth, root aerenchyma, and profiles of radial O2 loss (ROL) along adventitious roots were evaluated in 35 'wild' Hordeum accessions and cultivated barley (H. vulgare L. ssp. vulgare) when grown in stagnant nutrient solution (deoxygenated and containing 0.1% agar). When grown in stagnant solution, accessions from wetland and 'intermediate' habitats were superior, compared with accessions from non-wetland habitats, in maintaining relative growth rate, tillering, and adventitious root mass. Constitutive aerenchyma formation in adventitious roots was ≥10% in 22 accessions (cf. H. vulgare at 2%). When grown in stagnant solution, aerenchyma was ≥ 20% in the adventitious roots of 14 accessions (cf. H. vulgare at 12%). Variation among the accessions in the volume of aerenchyma formed when grown in aerated or stagnant solution was not determined by the waterlogging regime of the species' natural habitat. However, the genus Hordeum comprises four genomes and when grown in stagnant solution accessions with the X genome formed, on average, 22% aerenchyma in adventitious roots (50 mm behind apex), whereas those with the H genome averaged 19%, and those with the Y or I genomes averaged 16 and 15%, respectively. Sixteen accessions formed a barrier to ROL in the basal region of adventitious roots when grown in stagnant solution. The formation of a barrier to radial O2 loss was predominant in accessions from wet habitats, and absent in accessions from non-wetland habitats. In addition, this trait was only present in accessions with the X or H genomes. The combination of aerenchyma and a barrier to ROL enhances the longitudinal diffusion of O2 within roots towards the apex. The possibility of a link between having a barrier to ROL and the X or H genomes in Hordeum species might, in future studies, enable a genetic analysis of this important trait.

Evidence for the involvement of ethene in aerenchyma formation in adventitious roots of rice (Oryza sativa L.)

summaryTwo varieties of rice (ev. Norin 36 and RB3) were either grown in stagnant or aerated 1/4‐strength Hoagland's solution with or without exogenous ethene and a range of silver concentrations (an ethene antagonist), or were grown in flooded and drained soils.With cultivar Norin 36, AgNO3 was very effective in reducing porosity by inhibiting aerenchyma development. This effect was antagonized by gassing with increasing concentrations (1 or 2 μ1−l) of ethene. The results are consistent, therefore, with reports that cavity formation in roots is controlled by endogenous levels of ethene. Also, porosity varied with root length, and if a correction was made for this, the inhibitory effect of the silver ion on aerenchyma development appeared to be even greater.For the cultivar RB3, root porosities in solution culture appeared initially to be unaffected by ethene or AgNO2, but root lengths were reduced and root numbers increased by increasing ethene concentration. When these effects on root length were taken into account, it was concluded that ethene had increased root porosity, and AgNO3, had decreased it. Consistent with earlier studies, and with the ethene hypothesis, aerenchyma development in both varieties was also enhanced by soil waterlogging, with percentage porosities 12 units higher in flooded than in drained soil. The porosities of cv, RB3 were higher than those for cv. Norin 36, however, and the regression line of porosity against root length was steeper, indicating a greater predisposition to form aerenchyma in cv. RB3. This was confirmed in solution‐grown roots, where AgNO3 had no significant effect on porosity in stagnant or in aerated roots of cv. RB3, and both 1 and 2 μ1−1 ethene increased the porosity in cv. RB3 roots to a similar level. Silver nitrate, however, did antagonize the effects of 1 and 2 μ1−1 ethene. In contrast, porosity in cv. Norin 36 was progressively reduced by AgNO3.It is concluded that, although there are intervarietal differences in sensitivity, an ethene promotion of gas‐space formation can occur in rice, and ethene should not be ruled out as the endogenous promoter.