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Genetic and physiological aspects of barley (Hordeum vulgare L.) responses to waterlogging, salinity and aluminium stresses and their interactions

posted on 2023-05-27, 11:10 authored by Ma, Y
The term waterlogging‚ÄövÑvp is used to describe stressful conditions of root environment with excessive water, under which the diffusion of gases is reduced by almost four times of magnitude compared with that in the air. Decreased water and nutrient absorption by roots occurs with either complete (anoxia) or partial (hypoxia) depletion of oxygen. Waterlogging events may be a result of prolonged rain, flooding caused by melting snow, or poor soil drainage. The yield loss caused by waterlogging varies with duration of the stress, soil types and the tolerance of different species. The waterlogging stress could occur simultaneously with other soil stresses such as salinity which is another major abiotic stress that limits crop production via adverse effects of osmotic stress, specific ion toxicity, and stress-related nutritional disorders. Detrimental effects of salinity are often exacerbated by low oxygen availability when plants are grown under waterlogged conditions. In our study, we investigated the interaction between waterlogging and salinity stresses. A doubled haploid (DH) population consisting of 175 lines derived from a cross between a Chinese barley (Hordeum vulgare L.) variety Yangsimai 1 (YSM1) and an Australian malting barley variety Gairdner was used to construct a high density molecular map which contained more than 8,000 Diversity Arrays Technology (DArT) markers and single nucleotide polymorphism (SNP) markers. Salinity tolerance of parental and DH lines was evaluated under drained (SalinityD) and waterlogged (SalinityW) conditions at two different sowing times. Three quantitative trait loci (QTL) located on chromosome 1H, single QTL located on chromosome 1H, 2H, 4H, 5H and 7H, were identified to be responsible for salinity tolerance under different environments. Waterlogging stress, day length and temperature showed significant effects on barley salinity tolerance. The QTL for salinity tolerance mapped on chromosomes 4H (QSlwd.YG.4H) and 7H (QSlwd.YG.7H and QSlww.YG.7H) were only identified in winter trials, while the QTL on chromosome 2H (QSlsd.YG.2H and QSlsw.YG.2H) were only detected in summer trials. Genes associated with flowering time were found to pose significant effects on the salinity QTL mapped on chromosomes 2H and 5H in summer trials. Given the fact that two QTL for salinity tolerance on 1H, QSlsd.YG.1H and QSlww.YG.1H-1, reported here have never been considered in the literature, this warrants further investigation and evaluation for suitability to be used in breeding programs. Aluminium (Al) is prevalent in soils, but Al toxicity is manifested only in acid conditions. It causes severe damages to the root system. Short-term waterlogging stress can occur simultaneously with Al toxicity in areas with high rainfall or inappropriate irrigation pattern. In this work, we investigated effects of short-term treatments with hypoxia and phenolic acid (two major constraints in waterlogged soils) on roots' sensitivity to low-pH and Al stresses. We showed that hypoxia-primed roots maintained higher cell viability when exposed to low-pH/Al stress, in both elongation and mature root zones, and superior ability to retain K+ in response to low-pH/Al stresses. These priming effects were not related to higher H+-ATPase activity and better membrane potential maintenance, and could not be explained by the increased expression levels of HvHAK1, which mediates high-affinity K+ uptake in roots. Instead, hypoxia-conditioned roots were significantly less sensitive to H2O2 treatment, indicated by a 10-fold reduction in the magnitude of K+ efflux changes. This suggested that roots pre-treated with hypoxia desensitised ROS (reactive oxygen species)-inducible K+ efflux channels in root epidermis and had enhanced anti-oxidative capacity. A possible role of Ca2+ in stress-induced ROS signalling pathways is also discussed. We report, for the first time, the phenomenon of cross-protection between hypoxia and low-pH/Al stresses, and causally link it to cell's ability to maintain cytosolic K+ homeostasis. Barley is one of the most Al-sensitive small-grained cereals. The major gene for Al tolerance in barley is HvAACT1 (HvMATE) on chromosome 4H which encodes a multidrug and toxic compound extrusion (MATE) protein. The HvAACT1 protein facilitates the Al-activated release of citrate from root apices which protects the growing cells and enables root elongation to continue. A 1-kb transposable element-like insertion in the 5'-untranslated region (UTR) of HvAACT1 is associated with increased gene expression and Al tolerance and a PCR-based marker is available to score for this insertion. We screened a wide range of barley genotypes for Al tolerance and identified a moderately tolerant Chinese genotype named CXHKSL which did not show the typical allele in the 5'-UTR of HvAACT1 that is associated with tolerance. We investigated the mechanism of Al tolerance in CXHKSL and concluded that it also relies on the Al-activated release of citrate from roots. Quantitative trait loci (QTL) analysis of doubled haploid lines generated with CXHKSL and the Al-sensitive variety Gairdner mapped the tolerance locus to the same region as HvAACT1 on chromosome 4H. We found that the Chinese barley genotype CXHKSL possesses a novel allele of the major Al tolerance gene HvAACT1. In conclusion, a novel allele of the major Al tolerance gene HvAACT1 was identified from a Chinese variety. The allele also relies on the Al-activated release of citrate from roots. In addition, significant interactions between various stresses exist. Waterlogging stress increased the severity of salinity stress, while short-term waterlogging stress elevated barley tolerance to Al toxicity through ROS and Ca2+ signallings. Environmental conditions, for example, day length and temperature could pose significant effects on salinity tolerance. Therefore, both of those external (growth temperature, day length and soil water level) and internal factors (plant flowering time, cytosol ROS production, cytosol Ca2+ levels and allelic variation of tolerance genes) should be given significant emphasis when evaluating barley tolerance to either a specific abiotic stress or combined stresses.


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Copyright 2016 the Author Chapter 3 appears to be the equivalent of a post-print version of an article published as: Ma, YL, Shabala, S, Li, CD, Liu, CJ, Zhang, WY, Zhou, MX. 2015, Quantitative trait loci for salinity tolerance identified under drained and waterlogged conditions and their association with flowering time in barley (Hordeum vulgare L.). PLoS ONE, 10(8) Licensed under Creative Commons Attribution 4.0 International (CC BY 4.0) Chapter 4 appears to be the equivalent of a pre-copyedited, author-produced version of an article accepted for publication in: Plant and cell physiology following peer review. The version of record, Ma, YL, Zhu, M, Shabala, L, Zhou, MX, Shabala, S., 2016, Conditioning of roots with hypoxia increases aluminium and acid stress tolerance by mitigating activation of K+ efflux channels by ROS in barley: insights into cross-tolerance mechanisms. Plant Cell and Physiology, 57(1): 160-173 is available online at: Licensed under Creative Commons Attribution 4.0 International (CC BY 4.0) Chapter 5 appears to be the equivalent of a post-print version of an article published as: Ma, YL, Li, CD, Ryan, P, Shabala, S, You, JF, Liu, J, Liu, CJ, Zhou, MX. 2016, A new allele for the aluminium tolerance gene in barley (Hordeum vulgare L.). BMC Genomics, 2016, 17:186

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