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1.  The effects of induced production of reactive oxygen species in organelles on endoplasmic reticulum stress and on the unfolded protein response in arabidopsis 
Annals of Botany  2015;116(4):541-553.
Background and Aims Accumulation of unfolded proteins caused by inefficient chaperone activity in the endoplasmic reticulum (ER) is termed ‘ER stress’, and it is perceived by a complex gene network. Induction of these genes triggers a response termed the ‘unfolded protein response’ (UPR). If a cell cannot overcome the accumulation of unfolded proteins, the ER-associated degradation (ERAD) system is induced to degrade those proteins. In addition to other factors, reactive oxygen species (ROS) are also produced during oxidative protein-folding in the ER. It has been shown in animal systems that there is a tight association between mitochondrial ROS and ER stress. However, in plants there are no reports concerning how induced ROS production in mitochondria and chloroplasts affects ER stress and if there is a possible role of organelle-originated ROS as a messenger molecule in the unfolded protein response. To address this issue, electron transport in chloroplasts and mitochondria and carnitine acetyl transferase (CAT) activity in peroxisomes were inhibited in wild-type Arabidopsis thaliana to induce ROS production. Expression of UPR genes was then investigated.
Methods Plants of A. thaliana ecotype Col-0 were treated with various H2O2- and ROS-producing agents specific to different organelles, including the mitochondria, chloroplasts and peroxisomes. The expression of ER stress sensor/transducer genes (bZIP28, bZIP17, IRE1A, IRE1B, BiP1, BiP3), genes related to protein folding (CNX, ERO1) and ERAD genes (HRD1, SEL1, DER1, UBC32) were evaluated by qRT-PCR analysis.
Key Results Relatively low concentrations of ROS were more effective for induction of the ER stress response. Mitochondrial and chloroplastic ROS production had different induction mechanisms for the UPR and ER stress responses.
Conclusions Chloroplast- and mitochondria-originated ROS have distinct roles in triggering the ER stress response. In general, low concentrations of ROS induced the transcription of ER stress-related genes, which can be attributed to the roles of ROS as secondary messengers. This is the first time that ROS production in organelles has been shown to affect the ER stress response in a plant system.
PMCID: PMC4577994  PMID: 26070642
Oxidative stress; endoplasmic reticulum stress; unfolded protein response; UPR; endoplasmic reticulum-associated degradation; ERAD; reactive oxygen species; ROS; signalling; Arabidopsis thaliana
2.  Changes in the alternative electron sinks and antioxidant defence in chloroplasts of the extreme halophyte Eutrema parvulum (Thellungiella parvula) under salinity 
Annals of Botany  2014;115(3):449-463.
Background and Aims
Eutrema parvulum (synonym, Thellungiella parvula) is an extreme halophyte that thrives in high salt concentrations (100–150 mm) and is closely related to Arabidopsis thaliana. The main aim of this study was to determine how E. parvulum uses reactive oxygen species (ROS) production, antioxidant systems and redox regulation of the electron transport system in chloroplasts to tolerate salinity.
Plants of E. parvulum were grown for 30 d and then treated with either 50, 200 or 300 mm NaCl. Physiological parameters including growth and water relationships were measured. Activities of antioxidant enzymes were determined in whole leaves and chloroplasts. In addition, expressions of chloroplastic redox components such as ferrodoxin thioredoxin reductases (FTR), NADPH thioredoxin reductases (NTRC), thioredoxins (TRXs) and peroxiredoxins (PRXs), as well as genes encoding enzymes of the water–water cycle and proline biosynthesis were measured.
Key Results
Salt treatment affected water relationships negatively and the accumulation of proline was increased by salinity. E. parvulum was able to tolerate 300 mm NaCl over long periods, as evidenced by H2O2 content and lipid peroxidation. While Ca2+ and K+ concentrations were decreased by salinity, Na+ and Cl– concentrations increased. Efficient induction of activities and expressions of water–water cycle enzymes might prevent accumulation of excess ROS in chloroplasts and therefore protect the photosynthetic machinery in E. parvulum. The redox homeostasis in chloroplasts might be achieved by efficient induction of expressions of redox regulatory enzymes such as FTR, NTRC, TRXs and PRXs under salinity.
E. parvulum was able to adapt to osmotic stress by an efficient osmotic adjustment mechanism involving proline and was able to regulate its ion homeostasis. In addition, efficient induction of water–water cycle enzymes and other redox regulatory components such as TRXs and PRXs in chloroplasts were able to protect the chloroplasts from salinity-induced oxidative stress.
PMCID: PMC4332603  PMID: 25231894
Alternative electron sink; antioxidant enzymes; chloroplastic redox; Eutrema parvulum; halophyte; oxidative stress; peroxiredoxin; plastid terminal oxidase; proline; salinity; Thellungiella parvula; thioredoxin; water–water cycle
3.  Genetic diversity for grain nutrients in wild emmer wheat: potential for wheat improvement 
Annals of Botany  2010;105(7):1211-1220.
Background and Aims
Micronutrient malnutrition, particularly zinc and iron deficiency, afflicts over three billion people worldwide due to low dietary intake. In the current study, wild emmer wheat (Triticum turgidum ssp. dicoccoides), the progenitor of domesticated wheat, was tested for (1) genetic diversity in grain nutrient concentrations, (2) associations among grain nutrients and their relationships with plant productivity, and (3) the association of grain nutrients with the eco-geographical origin of wild emmer accessions.
A total of 154 genotypes, including wild emmer accessions from across the Near Eastern Fertile Crescent and diverse wheat cultivars, were characterized in this 2-year field study for grain protein, micronutrient (zinc, iron, copper and manganese) and macronutrient (calcium, magnesium, potassium, phosphorus and sulphur) concentrations.
Key Results
Wide genetic diversity was found among the wild emmer accessions for all grain nutrients. The concentrations of grain zinc, iron and protein in wild accessions were about two-fold greater than in the domesticated genotypes. Concentrations of these compounds were positively correlated with one another, with no clear association with plant productivity, suggesting that all three nutrients can be improved concurrently with no yield penalty. A subset of 12 populations revealed significant genetic variation between and within populations for all minerals. Association between soil characteristics at the site of collection and grain nutrient concentrations showed negative associations between soil clay content and grain protein and between soil-extractable zinc and grain zinc, the latter suggesting that the greatest potential for grain nutrient minerals lies in populations from micronutrient-deficient soils.
Wild emmer wheat germplasm offers unique opportunities to exploit favourable alleles for grain nutrient properties that were excluded from the domesticated wheat gene pool.
PMCID: PMC2887062  PMID: 20202969
grain quality; iron; macronutrient; micronutrient; protein; Triticum turgidum ssp. dicoccoides; wheat improvement; zinc
4.  Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa) 
Annals of Botany  2008;103(2):197-209.
Background and Aims
Flooding slows seed germination, imposes fatalities and delays seedling establishment in direct-seeded rice. This study describes responses of contrasting rice genotypes subjected to flooding or low oxygen stress during germination and discusses the basis of tolerance shown by certain cultivars.
In one set of experiments, dry seeds were sown in soil and either watered normally or flooded with 10 cm of water. Seedling survival and shoot and root growth were assessed and seed portions of germinating seedlings were assayed for soluble sugars and starch concentrations. The whole germinating seedlings were assayed for amylase and peroxidase activities and for ethylene production. Activities of enzymes associated with anaerobic respiration were examined and gene expression was analysed separately with seeds germinating under different amounts of dissolved oxygen in dilute agar.
Key Results
Flooding during germination reduced survival but to a lesser extent in tolerant genotypes. Starch concentration in germinating seeds decreased while sugar concentration increased under flooding, but more so in tolerant genotypes. Amylase activity correlated positively with elongation (r = 0·85 for shoot and 0·83 for root length) and with plant survival (r = 0·92). Tolerant genotypes had higher amylase activity and higher RAmy3D gene expression. Ethylene was not detected in seeds within 2 d after sowing, but increased thereafter, with a greater increase in tolerant genotypes starting 3 d after sowing. Peroxidase activity was higher in germinating seeds of sensitive genotypes and correlated negatively with survival.
Under low oxygen stress, tolerant genotypes germinate, grow faster and more seedlings survive. They maintain their ability to use stored starch reserves through higher amylase activity and anaerobic respiration, have higher rates of ethylene production and lower peroxidase activity as germinating seeds and as seedlings. Relevance of these traits to tolerance of flooding during germination and early growth is discussed.
PMCID: PMC2707318  PMID: 19001425
Amylase; anoxia; crop establishment; direct-seeded rice; ethylene; flooding; germination; hypoxia; Oryza sativa
5.  Development of submergence-tolerant rice cultivars: the Sub1 locus and beyond 
Annals of Botany  2008;103(2):151-160.
Background and Aims
Submergence is a recurring problem in the rice-producing rainfed lowlands of south and south-east Asia. Developing rice cultivars with tolerance of submergence and with agronomic and quality traits acceptable to farmers is a feasible approach to address this problem. The objectives of this study were to (a) develop mega varieties with Sub1 introgression that are submergence tolerant, (b) assess the performance of Sub1 in different genetic backgrounds, (c) determine the roles of the Sub1A and Sub1C genes in conferring tolerance, and (d) assess the level of tolerance in F1 hybrids heterozygous for the Sub1A-1-tolerant allele.
Tolerant varieties were developed by marker-assisted backcrossing through two or three backcrosses, and their performance was evaluated to determine the effect of Sub1 in different genetic backgrounds. The roles of Sub1A and Sub1C in conferring the tolerant phenotype were further investigated using recombinants identified within the Sub1 gene cluster based on survival and gene expression data.
Key Results
All mega varieties with Sub1 introgression had a significantly higher survival rate than the original parents. An intolerant Sub1C allele combined with the tolerant Sub1A-1 allele did not significantly reduce the level of tolerance, and the Sub1C-1 expression appeared to be independent of the Sub1A allele; however, even when Sub1C-1 expression is completely turned off in the presence of Sub1A-2, plants remained intolerant. Survival rates and Sub1A expression were significantly lower in heterozygotes compared with the homozygous tolerant parent.
Sub1 provided a substantial enhancement in the level of tolerance of all the sensitive mega varieties. Sub1A is confirmed as the primary contributor to tolerance, while Sub1C alleles do not seem important. Lack of dominance of Sub1 suggests that the Sub1A-1 allele should be carried by both parents for developing tolerant rice hybrids.
PMCID: PMC2707316  PMID: 18974101
Oryza sativa; Sub1; marker-assisted backcrossing; mega varieties; submergence tolerance; recombinant; hybrid; abiotic stress
6.  Adaptation to flooding in upland and lowland ecotypes of Cyperus rotundus, a troublesome sedge weed of rice: tuber morphology and carbohydrate metabolism 
Annals of Botany  2008;103(2):295-302.
Background and aims
In recent years, Cyperus rotundus has become a problem weed in lowland rice (Oryza sativa) grown in rotation with vegetables in the Philippines. As the growth of C. rotundus is commonly suppressed by prolonged flooding, the ability of the weed to grow vigorously in flooded as well as upland conditions suggests that adapted ecotypes occur in these rotations. Studies were conducted to elucidate the mechanisms that permit C. rotundus to tolerate flooded soil conditions.
Upland and lowland ecotypes of C. rotundus were compared in terms of growth habit, carbohydrate reserves and metabolism, and activities of enzymes involved in alcoholic fermentation – alcohol dehydrogenase (ADH) and pyruvate decarboxylase (PDC).
Key Results
The lowland ecotype has much larger tubers than the upland ecotype. Prior to germination, the amylase activity and total non-structural carbohydrate content in the form of soluble sugars were greater in the tubers of lowland plants than in those of upland C. rotundus. At 24 h after germination in hypoxic conditions, PDC and ADH activities in the lowland plants increased, before decreasing at 48 h following germination. In contrast, ADH and PDC activities in the upland plants increased from 24 to 48 h after germination.
Tolerance of lowland C. rotundus of flooding may be attributed to large carbohydrate content and amylase activity, and the ability to maintain high levels of soluble sugars in the tubers during germination and early growth. This is coupled with the modulation of ADH and PDC activities during germination, possibly to control the use of carbohydrate reserves and sustain substrate supply in order to avoid starvation and death of seedlings with prolonged flooding.
PMCID: PMC2707299  PMID: 18515404
Anoxia; ethanol fermentation; flooding tolerance; nutsedge; Cyperus rotundus; Pasteur effect; weed ecology
7.  Responses of Photosynthesis, Chlorophyll Fluorescence and ROS-Scavenging Systems to Salt Stress During Seedling and Reproductive Stages in Rice 
Annals of Botany  2007;99(6):1161-1173.
Background and Aims
Salinity is a widespread soil problem limiting productivity of cereal crops worldwide. Rice is particularly sensitive to salt stress during the seedling stage, with consequent poor crop establishment, as well as during reproduction where salinity can severely disrupt grain formation and yield. Tolerance at the seedling stage is weakly associated with tolerance during reproduction. Physiological responses to salinity were evaluated for contrasting genotypes, during the seedling and reproductive stages.
Three rice genotypes differing in their tolerance of salinity were evaluated in a set of greenhouse experiments under salt stress during both seedling stage and reproduction.
Key Results
Photosynthetic CO2 fixation, stomatal conductance (gs) and transpiration decreased substantially because of salt stress, but with greater reduction in the sensitive cultivar IR29. The tolerant lines IR651 and IR632 had more responsive stomata that tended to close faster during the first few hours of stress, followed by partial recovery after a brief period of acclimation. However, in the sensitive line, gs continued to decrease for longer duration and with no recovery afterward. Chlorophyll fluorescence measurements revealed that non-photochemical quenching increased, whereas the electron transport rate decreased under salt stress. Salt-tolerant cultivars exhibited much lower lipid peroxidation, maintained elevated levels of reduced ascorbic acid and showed increased activities of the enzymes involved in the reactive oxygen scavenging system during both developmental stages.
Upregulation of the anti-oxidant system appears to play a role in salt tolerance of rice, with tolerant genotypes also maintaining relatively higher photosynthetic function; during both the vegetative and reproductive stages.
PMCID: PMC3243573  PMID: 17428832
Chlorophyll fluorescence; photosynthesis; reactive oxygen species; rice; Oryza sativa; salinity

Results 1-7 (7)