Late Embryogenesis Abundant (LEA)5 Regulates Translation in Mitochondria and Chloroplasts to Enhance Growth and Stress Tolerance

Karpińska, Barbara; Razak, Nurhayati; Shaw, Daniel S.; Plumb, William J.; Slijke, Eveline Van De; Stephens, Jennifer; Jaeger, Geert De; Murcha, Monika W.; Foyer, Christine H.

doi:10.3389/fpls.2022.875799

Cited by 16 publications

(14 citation statements)

References 46 publications

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“…In SEG, this gene is significantly up-regulated in Topas only (log2 fold change of 1.28). Similarly, SENESCENCE-ASSOCIATED GENE 21/LATE EMBRYONIC ABUNDANT 5 ( SAG21 / LEA5 ) plays a specific protective role against oxidative stress by repressing photosynthesis [ 13 , 14 ] and displays the highest heat-induced response in Topas seeds (log2 fold change of 4.15 and 3.55 in SE8 and SEG, respectively).…”

Section: Resultsmentioning

confidence: 99%

Transcriptome analysis of thermomorphogenesis in ovules and during early seed development in Brassica napus

et al. 2023

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Background Plant sexual reproduction is highly sensitive to elevated ambient temperatures, impacting seed development and production. We previously phenotyped this effect on three rapeseed cultivars (DH12075, Topas DH4079, and Westar). This work describes the transcriptional response associated with the phenotypic changes induced by heat stress during early seed development in Brassica napus. Results We compared the differential transcriptional response in unfertilized ovules and seeds bearing embryos at 8-cell and globular developmental stages of the three cultivars exposed to high temperatures. We identified that all tissues and cultivars shared a common transcriptional response with the upregulation of genes linked to heat stress, protein folding and binding to heat shock proteins, and the downregulation of cell metabolism. The comparative analysis identified an enrichment for a response to reactive oxygen species (ROS) in the heat-tolerant cultivar Topas, correlating with the phenotypic changes. The highest heat-induced transcriptional response in Topas seeds was detected for genes encoding various peroxidases, temperature-induced lipocalin (TIL1), or protein SAG21/LEA5. On the contrary, the transcriptional response in the two heat-sensitive cultivars, DH12075 and Westar, was characterized by heat-induced cellular damages with the upregulation of genes involved in the photosynthesis and plant hormone signaling pathways. Particularly, the TIFY/JAZ genes involved in jasmonate signaling were induced by stress, specifically in ovules of heat-sensitive cultivars. Using a weighted gene co-expression network analysis (WGCNA), we identified key modules and hub genes involved in the heat stress response in studied tissues of either heat-tolerant or sensitive cultivars. Conclusions Our transcriptional analysis complements a previous phenotyping analysis by characterizing the growth response to elevated temperatures during early seed development and reveals the molecular mechanisms underlying the phenotypic response. The results demonstrated that response to ROS, seed photosynthesis, and hormonal regulation might be the critical factors for stress tolerance in oilseed rape.

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Section: Resultsmentioning

confidence: 99%

Transcriptome analysis of thermomorphogenesis in ovules and during early seed development in Brassica napus

et al. 2023

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“…Other systems may operate to regulate chloroplast translation in response to oxidative signals. For example, the expression of late embryogenesis abundant 5 (LEA5) protein is induced by oxidative stress but not by light (Karpinska et al., 2022). LEA5 plays an important in the downregulation of photosynthesis in Arabidopsis plants exposed to stress by regulating organellar translation.…”

Section: Thioredoxin‐dependent Control Of Electron Transport Processesmentioning

confidence: 99%

“…LEA5 plays an important in the downregulation of photosynthesis in Arabidopsis plants exposed to stress by regulating organellar translation. Expression of this protein leads to inhibition of translation in chloroplasts but conversely stimulates translation in mitochondria (Karpinska et al., 2022).…”

Section: Thioredoxin‐dependent Control Of Electron Transport Processesmentioning

confidence: 99%

ROS production and signalling in chloroplasts: cornerstones and evolving concepts

2022

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Reactive oxygen species (ROS) such as singlet oxygen, superoxide (O 2•À ) and hydrogen peroxide (H 2 O 2 ) are the markers of living cells. Oxygenic photosynthesis produces ROS in abundance, which act as a readout of a functional electron transport system and metabolism. The concept that photosynthetic ROS production is a major driving force in chloroplast to nucleus retrograde signalling is embedded in the literature, as is the role of chloroplasts as environmental sensors. The different complexes and components of the photosynthetic electron transport chain (PETC) regulate O 2 •À production in relation to light energy availability and the redox state of the stromal Cys-based redox systems. All of the ROS generated in chloroplasts have the potential to act as signals and there are many sulphhydryl-containing proteins and peptides in chloroplasts that have the potential to act as H 2 O 2 sensors and function in signal transduction. While ROS may directly move out of the chloroplasts to other cellular compartments, ROS signalling pathways can only be triggered if appropriate ROS-sensing proteins are present at or near the site of ROS production. Chloroplast antioxidant systems serve either to propagate these signals or to remove excess ROS that cannot effectively be harnessed in signalling. The key challenge is to understand how regulated ROS delivery from the PETC to the Cys-based redox machinery is organised to transmit redox signals from the environment to the nucleus. Redox changes associated with stromal carbohydrate metabolism also play a key role in chloroplast signalling pathways.

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“…This gene was found to be upregulated in the tolerant pearl millet genotype under drought stress. Arabidopsis plants that overexpressed AtLEA5 showed tolerance to oxidative stress and overexpression of AtLEA5 in barley lead to increased seed yield (Karpinska et al, 2022). LEA5 regulates organellar translation, to enhance respiration relative to photosynthesis in response to stress (Karpinska et al, 2022).…”

Section: Insight Into Pearl Millet Drought Tolerant Mechanisms Using ...mentioning

confidence: 99%

“…Arabidopsis plants that overexpressed AtLEA5 showed tolerance to oxidative stress and overexpression of AtLEA5 in barley lead to increased seed yield (Karpinska et al, 2022). LEA5 regulates organellar translation, to enhance respiration relative to photosynthesis in response to stress (Karpinska et al, 2022). Introduction of LEA protein genes into spring wheat also significantly increased water use efficiency compared to non-transgenic lines under water deficit conditions (Sivamani et al, 2000).…”

Section: Insight Into Pearl Millet Drought Tolerant Mechanisms Using ...mentioning

confidence: 99%

Pearl millet response to drought: A review

Shrestha

Hu²,

Shrestha³

et al. 2023

Front. Plant Sci.

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The C4 grass pearl millet is one of the most drought tolerant cereals and is primarily grown in marginal areas where annual rainfall is low and intermittent. It was domesticated in sub-Saharan Africa, and several studies have found that it uses a combination of morphological and physiological traits to successfully resist drought. This review explores the short term and long-term responses of pearl millet that enables it to either tolerate, avoid, escape, or recover from drought stress. The response to short term drought reveals fine tuning of osmotic adjustment, stomatal conductance, and ROS scavenging ability, along with ABA and ethylene transduction. Equally important are longer term developmental plasticity in tillering, root development, leaf adaptations and flowering time that can both help avoid the worst water stress and recover some of the yield losses via asynchronous tiller production. We examine genes related to drought resistance that were identified through individual transcriptomic studies and through our combined analysis of previous studies. From the combined analysis, we found 94 genes that were differentially expressed in both vegetative and reproductive stages under drought stress. Among them is a tight cluster of genes that are directly related to biotic and abiotic stress, as well as carbon metabolism, and hormonal pathways. We suggest that knowledge of gene expression patterns in tiller buds, inflorescences and rooting tips will be important for understanding the growth responses of pearl millet and the trade-offs at play in the response of this crop to drought. Much remains to be learnt about how pearl millet’s unique combination of genetic and physiological mechanisms allow it to achieve such high drought tolerance, and the answers to be found may well be useful for crops other than just pearl millet.

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Late Embryogenesis Abundant (LEA)5 Regulates Translation in Mitochondria and Chloroplasts to Enhance Growth and Stress Tolerance

Cited by 16 publications

References 46 publications

Transcriptome analysis of thermomorphogenesis in ovules and during early seed development in Brassica napus

Transcriptome analysis of thermomorphogenesis in ovules and during early seed development in Brassica napus

ROS production and signalling in chloroplasts: cornerstones and evolving concepts

Pearl millet response to drought: A review

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