ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) affects development, photosynthesis, and hormonal homeostasis in hybrid aspen ( Populus tremula L. ×  P. tremuloides )

Bernacki, Maciej Jerzy; Czarnocka, Weronika; Witoń, Damian; Rusaczonek, Anna; Szechyńska‐Hebda, Magdalena; Ślesak, Ireneusz; Dąbrowska-Bronk, Joanna; Karpiński, Stanisław

doi:10.1016/j.jplph.2018.04.014

Cited by 14 publications

(21 citation statements)

References 93 publications

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“…The exact role and function of the identified genes is not known; however, they could be interesting candidates for future experiments, especially Syntaxin-122 (SYP122), which negatively regulates runaway CD, depending on LSD1 and EDS1; BT2 and BT4, which are connected to the hormonal signalling, and apparently function in integrating biotic and abiotic stresses signals; MYB73, which participates in NPR1-mediated JA and SA signalling pathways; and ELIP1, which belongs to the multigene family of pigment-binding LHCII and, therefore, prevents photo-oxidative damage. These results strongly confirm our previous reports and working model concerning the role of NPQ, LHCII arrangement, LSD1 and EDS1conditional molecular regulators in chloroplast retrograde signalling and the nuclear anterograde response in simultaneous regulation of light acclimatory and immune defence responses (Bernacki et al, 2018;Karpi nski et al, 2013;Mateo et al, 2004;Mühlenbock et al, 2008;Szechy nska-Hebda et al, 2010;Wituszy nska et al, 2013Wituszy nska et al, , 2015.…”

Section: Discussionsupporting

confidence: 92%

“…Moreover, its role is clear in the up‐regulation of water‐use efficiency (Correa‐Galvis et al, ). On the other hand, our previous experiments have demonstrated that NPQ and LHCII arrangement, together with CD conditional molecular regulators ( lesion‐simulating disease [ LSD1 ], enhanced disease susceptibility [ EDS1 ]), play a key role in chloroplast retrograde electrical and biochemical signalling as well as in anterograde regulation of light memory, and thus, in the proper induction of SAA, SAR, water‐use efficiency and CD (Bernacki et al, ; Karpiński et al, ; Mateo et al, ; Mühlenbock et al, ; Szechyńska‐Hebda et al, ; Wituszyńska et al, , ). Considering the fact that growth, development and plant productivity responses are dependent on photosynthesis, chloroplast retrograde signalling, cell‐cycle regulation and the ultimate end of the cell cycle (CD), we formulated a working hypothesis that PsbS plays an important role in direct or indirect regulation of light memory, chloroplast retrograde redox and electrical signalling, light acclimation, and cross‐tolerance to UV.…”

Section: Resultsmentioning

confidence: 99%

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Photosystem II 22kDa protein level ‐ a prerequisite for excess light‐inducible memory, cross‐tolerance to UV‐C and regulation of electrical signalling

Górecka

Lewandowska

Dąbrowska-Bronk

et al. 2020

Plant Cell & Environment

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It is well known that PsbS is a key protein for the proper management of excessive energy in plants. Plants without PsbS cannot trigger non‐photochemical quenching, which is crucial for optimal photosynthesis under variable conditions. Our studies showed wild‐type plants had enhanced tolerance to UV‐C‐induced cell death (CD) upon induction of light memory by a blue or red light. However, npq4‐1 plants, which lack PsbS, as well as plants overexpressing this protein (oePsbS), responded differently. Untreated oePsbS appeared more tolerant to UV‐C exposure, whereas npq4‐1 was unable to adequately induce cross‐tolerance to UV‐C. Similarly, light memory induced by episodic blue or red light was differently deregulated in npq‐4 and oePsbS, as indicated by transcriptomic analyses, measurements of the trans‐thylakoid pH gradient, chlorophyll a fluorescence parameters, and measurements of foliar surface electrical potential. The mechanism of the foliar CD development seemed to be unaffected in the analysed plants and is associated with chloroplast breakdown. Our results suggest a novel, substantial role for PsbS as a regulator of chloroplast retrograde signalling for light memory, light acclimation, CD, and cross‐tolerance to UV radiation.

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Section: Discussionsupporting

confidence: 92%

Section: Resultsmentioning

confidence: 99%

Photosystem II 22kDa protein level ‐ a prerequisite for excess light‐inducible memory, cross‐tolerance to UV‐C and regulation of electrical signalling

Górecka

Lewandowska

Dąbrowska-Bronk

et al. 2020

Plant Cell & Environment

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“…Furthermore, LSD1 is a condition‐dependent scaffold protein and transcription regulator, and forms dimers with EDS1 (Czarnocka et al ). Recently, we reported that PAD4 and EDS1 can function in woody plants in a similar manner as in Arabidopsis (Ślesak et al , Szechyńska‐Hebda et al , Bernacki et al ).…”

Section: Introductionmentioning

confidence: 77%

“…Salicylic acid (SA) and reactive oxygen species (ROS), such as H 2 O 2 , are important signaling molecules that regulate CD, photosynthesis, WUE, stomatal conductance and cross‐tolerance processes (Desikan et al , Gechev and Hille , Ślesak et al , Wituszyńska et al , Wituszyńska et al , Szechyńska‐Hebda et al , Bernacki et al , Czarnocka and Karpiński ). They also play a vital role in plant development (Mittler et al , Gawroński et al ) and seed yield control (Abreu and Munné‐Bosch ).…”

Section: Introductionmentioning

confidence: 99%

LSD1‐, EDS1‐ and PAD4‐dependent conditional correlation among salicylic acid, hydrogen peroxide, water use efficiency and seed yield in Arabidopsis thaliana

Bernacki

Czarnocka

Rusaczonek

et al. 2019

Physiologia Plantarum

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In Arabidopsis thaliana, LESION SIMULATING DISEASE 1 (LSD1), ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) and PHYTOALEXIN DEFICIENT 4 (PAD4) proteins are regulators of cell death (CD) in response to abiotic and biotic stresses. Hormones, such as salicylic acid (SA), and reactive oxygen species, such as hydrogen peroxide (H2O2), are key signaling molecules involved in plant CD. The proposed mathematical models presented in this study suggest that LSD1, EDS1 and PAD4 together with SA and H2O2 are involved in the control of plant water use efficiency (WUE), vegetative growth and generative development. The analysis of Arabidopsis wild‐type and single mutants lsd1, eds1, and pad4, as well as double mutants eds1/lsd1 and pad4/lsd1, demonstrated the strong conditional correlation between SA/H2O2 and WUE that is dependent on LSD1, EDS1 and PAD4 proteins. Moreover, we found a strong correlation between the SA/H2O2 homeostasis of 4‐week‐old Arabidopsis leaves and a total seed yield of 9‐week‐old plants. Altogether, our results prove that SA and H2O2 are conditionally regulated by LSD1/EDS/PAD4 to govern WUE, biomass accumulation and seed yield. Conditional correlation and the proposed models presented in this study can be used as the starting points in the creation of a plant breeding algorithm that would allow to estimate the seed yield at the initial stage of plant growth, based on WUE, SA and H2O2 content.

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“…The roles of several stress response genes in regulating photosynthesis have been identified via transgenic analysis in perennial trees. For example, silencing the expression of the stress response gene ENHANCED DISEASE SUSCEPTIBILITY1 ( EDS1 ) improved the quantum yield of photosystem II and chlorophyll content in hybrid Populus ( Populus tremula L. × P. tremuloides ) (Bernacki et al , ). Although several studies have demonstrated the important roles of various individual genes in the photosynthetic pathway, the genetic architecture of the targeted photosynthesis‐related traits remains unknown, especially the magnitude of the genetic effects of causal genes and alleles, as well as the allelic interactions among genes involved in the photosynthetic pathway.…”

Section: Introductionmentioning

confidence: 99%

Genetic dissection of the gene coexpression network underlying photosynthesis in Populus

Liang

Liu

et al. 2019

Plant Biotechnology Journal

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Summary Photosynthesis is a key reaction that ultimately generates the carbohydrates needed to form woody tissues in trees. However, the genetic regulatory network of protein‐encoding genes (PEGs) and regulatory noncoding RNAs (ncRNAs), including microRNAs (miRNAs) and long noncoding RNAs (lncRNAs), underlying the photosynthetic pathway is unknown. Here, we integrated data from coexpression analysis, association studies (additive, dominance and epistasis), and expression quantitative trait nucleotide (eQTN) mapping to dissect the causal variants and genetic interaction network underlying photosynthesis in Populus. We initially used 30 PEGs, 6 miRNAs and 12 lncRNAs to construct a coexpression network based on the tissue‐specific gene expression profiles of 15 Populus samples. Then, we performed association studies using a natural population of 435 unrelated Populus tomentosa individuals, and identified 72 significant associations (P ≤ 0.001, q ≤ 0.05) with diverse additive and dominance patterns underlying photosynthesis‐related traits. Analysis of epistasis and eQTNs revealed that the complex genetic interactions in the coexpression network contribute to phenotypes at various levels. Finally, we demonstrated that heterologously expressing the most highly linked gene (PtoPsbX1) in this network significantly improved photosynthesis in Arabidopsis thaliana, pointing to the functional role of PtoPsbX1 in the photosynthetic pathway. This study provides an integrated strategy for dissecting a complex genetic interaction network, which should accelerate marker‐assisted breeding efforts to genetically improve woody plants.

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ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) affects development, photosynthesis, and hormonal homeostasis in hybrid aspen ( Populus tremula L. ×  P. tremuloides )

Cited by 14 publications

References 93 publications

Photosystem II 22kDa protein level ‐ a prerequisite for excess light‐inducible memory, cross‐tolerance to UV‐C and regulation of electrical signalling

Photosystem II 22kDa protein level ‐ a prerequisite for excess light‐inducible memory, cross‐tolerance to UV‐C and regulation of electrical signalling

LSD1‐, EDS1‐ and PAD4‐dependent conditional correlation among salicylic acid, hydrogen peroxide, water use efficiency and seed yield in Arabidopsis thaliana

Genetic dissection of the gene coexpression network underlying photosynthesis in Populus

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ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) affects development, photosynthesis, and hormonal homeostasis in hybrid aspen ( Populus tremula L. × P. tremuloides )

Cited by 14 publications

References 93 publications

Photosystem II 22kDa protein level ‐ a prerequisite for excess light‐inducible memory, cross‐tolerance to UV‐C and regulation of electrical signalling

Photosystem II 22kDa protein level ‐ a prerequisite for excess light‐inducible memory, cross‐tolerance to UV‐C and regulation of electrical signalling

LSD1‐, EDS1‐ and PAD4‐dependent conditional correlation among salicylic acid, hydrogen peroxide, water use efficiency and seed yield in Arabidopsis thaliana

Genetic dissection of the gene coexpression network underlying photosynthesis in Populus

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Product

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ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) affects development, photosynthesis, and hormonal homeostasis in hybrid aspen ( Populus tremula L. ×  P. tremuloides )