A stress recovery signaling network for enhanced flooding tolerance in
            <i>Arabidopsis thaliana</i>

Yeung, Euson; Veen, Hans van; Vashisht, Divya; Paiva, Ana Luiza Sobral; Hummel, Maureen; Rankenberg, Tom; Steffens, Bianka; Steffen‐Heins, Anja; Sauter, Margret; Vries, Michèl de; Schuurink, Robert C.; Bazin, Jérémie; Bailey‐Serres, Julia; Voesenek, Laurentius A. C. J.; Sasidharan, Rashmi

doi:10.1073/pnas.1803841115

Cited by 141 publications

(113 citation statements)

References 60 publications

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“…Chlorophyll retention during submergence was positively linked to RGR upon de-submergence both in basal and apical leaves as indicated by the registered leaf greenness dynamics. In this respect, the more tolerant genotypes of L. japonicus (RILs 18, 30, and 189) presented lower amounts of (or high sensitivity to) reactive oxygen species (ROS) upon re-aeration (i.e., less oxidative stress), low ethylene formation, and diminished leaf dehydration during recovery compared to the more susceptible ones (RILs 6, 47 and Gifu), similar to what was reported in contrasting accessions of Arabidopsis thaliana for submergence tolerance (accessions Lp2-6 vs. Bay-0; [13]). Interestingly, all L. japonicus genotypes showed similarly low values for Fv/Fm in young fully expanded leaves, indicating damage to the Photosystem II (PSII) two days after de-submergence.…”

Section: Discussionsupporting

confidence: 69%

“…Carbon assimilation and growth after de-submergence are influenced by the degree of stomata aperture enabling diffusion of carbon dioxide towards chloroplasts, the N status of leaves, and the functional degree of the photosynthetic apparatus (if damaged) [13,26,38]. In this study, we registered differences among genotypes in stomatal conductance (g s ), where genotypes with high S:R and low leaf RWC showed lower values of g s until showing recovery for this parameter during the second week after de-submergence.…”

Section: Discussionmentioning

confidence: 99%

“…Plant responses during submergence have been extensively studied and documented [4,[9][10][11][12], while plant responses after water recession (i.e. recovery phase) have seldom been reported (but see [13,14] for Arabidopsis thaliana). This study aims at identifying eco-physiological traits facilitating plant recovery after complete submergence.Forage legumes are important components of pastures and natural grasslands.…”

mentioning

confidence: 99%

“…Pioneer works [26,27] showed that the ability to resume growth after 20 days of submergence in the forb Alternanthera philoxeroides and the grass Hemarthria altissima resulted from rapid leaf growth and recovery of functionality of the photosynthetic apparatus. In two contrasting accessions for submergence tolerance of Arabidopsis thaliana (Bay-0-sensitive vs. Lp2-tolerant), it was shown that quick stomatal aperture, higher chlorophyll retention, and leaf water turgor maintenance were key factors for the tolerant accession to sustain a fast recovery following the removal of the stress [13], these traits also provide a detailed recovery-signaling network for enhanced flooding tolerance in Arabidopsis. In this study, we selected 10 RILs of L. japonicus (plus both parents) with differential constitutive shoot to root dry mass ratios (S:R) from [23] with the objective to assess leaf water status, stomatal conductance, dark-adapted chlorophyll fluorescence of photosystem II (Fv/Fm), Plants 2020, 9, 538 3 of 19 and greenness of basal and apical leaves (as a surrogate to infer N status) and explore how these variables correlate with plant growth resumption (i.e., plant RGR: relative growth rate).…”

mentioning

confidence: 99%

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Eco-Physiological Traits Related to Recovery from Complete Submergence in the Model Legume Lotus japonicus

Buraschi

Mollard

Grimoldi

et al. 2020

Plants

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Submergence is a severe form of stress for most plants. Lotus japonicus is a model legume with potential use in assisting breeding programs of closely related forage Lotus species. Twelve L. japonicus genotypes (10 recombinant inbred lines (RILs) and 2 parental accessions) with different constitutive shoot to root dry mass ratios (S:R) were subjected to 7 days of submergence in clear water and allowed to recover for two weeks post-submergence; a set of non-submerged plants served as controls. Relative growth rate (RGR) was used to indicate the recovery ability of the plants. Leaf relative water content (RWC), stomatal conductance (g s ), greenness of basal and apical leaves, and chlorophyll fluorescence (Fv/Fm, as a measure of photoinhibition) were monitored during recovery, and relationships among these variables and RGR were explored across genotypes. The main results showed (i) variation in recovery ability (RGR) from short-term complete submergence among genotypes, (ii) a trade-off between growth during vs. after the stress indicated by a negative correlation between RGR during submergence and RGR post-submergence, (iii) an inverse relationship between RGR during recovery and S:R upon de-submergence, (iv) positive relationships between RGR at early recovery and RWC and g s , which were negatively related to S:R, suggesting this parameter as a good estimator of plant water balance post-submergence, (v) chlorophyll retention allowed fast recovery as revealed by the positive relationship between greenness of basal and apical leaves and RGR during the first recovery week, and (vi) full repair of the submergence-damaged photosynthetic apparatus occurred more slowly (second recovery week) than full recovery of plant water relations. The inclusion of these traits contributing to submergence recovery in L. japonicus should be considered to speed up the breeding process of the closely related forage Lotus spp. used in current agriculture.Plants 2020, 9, 538 2 of 19 plants confront in prone-to-flood environments [2]. This situation drastically decreases the direct exchange of gases between the plant and the atmosphere, resulting in reduced O 2 and CO 2 levels [3]. Moreover, complete submergence often reduces the irradiance for photosynthesis depending on the water depth and turbidity. Two plant strategies have been recognized in plant submergence responses: (i) the "escape strategy" and (ii) the "quiescent' strategy" [4][5][6]. The first one involves shoot elongation to restore leaf contact with the atmosphere and offers plants a better chance to survive under shallow long-term submergence (>1 week). The "quiescent" strategy is based on maintaining steady energy conservation without shoot elongation and it is usually adopted to cope with deep short-term submergence (<1 week), given that shoot emergence represents a high energy cost that could compromise subsequent plant recovery [3,7]. Thus, in scenarios of short, deep submergence with low CO 2 and/or low light, plants rarely grow, but instead aim just to survive until...

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Section: Discussionsupporting

confidence: 69%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Eco-Physiological Traits Related to Recovery from Complete Submergence in the Model Legume Lotus japonicus

Buraschi

Mollard

Grimoldi

et al. 2020

Plants

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“…Ethylene mainly inhibits ABA signaling but activates ABA-independent dehydration regulators including several dehydration-responsive element-binding (DREB) transcription factors (Tfs) including (CBF1 (C-repeat binding factors), TINY, HARDY). 24,25 AP2/ERFs (Apelata2/ Ethylene response factors) are one of the most important Tf families in plants which control different biotic and abiotic stress responsive pathways. 26,27 Based on DNA binding domain (DBD), AP2/ERFs are further divided into AP2, RAV (Related to Abscisic acid insensitive3/Viviparous1), DREB (subgroup A1-A6), ERF (subgroup B1-B6), and others.…”

Section: Post-waterlogging Stress In Plantsmentioning

confidence: 99%

Hormone dependent survival mechanisms of plants during post-waterlogging stress

Bashar

2018

Plant Signaling & Behavior

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Waterlogging stress has two phases like waterlogging phase and post-waterlogging phase where both are injurious to plants. Susceptible plants normally die at post-waterlogging phase due to damaged root system, sudden rexoygenation, dehydration and photoinhibition of the desubmerged tissues. Formation of reactive oxygen species (ROS) is the main result of reoxygenation stress that can cause oxidative damage of the functional tissues responsible for normal physiological activities. There are almost all types of hormones responsible to recover plants from these destructive phenomenons. Among these hormones ethylene and abscisic acid (ABA) are the main regulators to overcome the reoxygenation and drought like stresses in plants at post-waterlogging condition. The balanced crosstalk among the hormones is highly important for the survival of plants at these stresses. So this paper is completely a precise summary of hormonal homeostasis of post-waterlogged plants through physiological, biochemical and signaling pathways. ARTICLE HISTORY

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Flood resilience loci SUBMERGENCE 1 and ANAEROBIC GERMINATION 1 interact in seedlings established underwater

et al. 2020

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Crops with resilience to multiple climatic stresses are essential for increased yield stability. Here, we evaluate the interaction between two loci associated with flooding survival in rice ( Oryza sativa L.). ANAEROBIC GERMINATION 1 ( AG1 ), encoding trehalose 6‐phosphate phosphatase 7 ( TPP7 ), promotes mobilization of endosperm reserves to enhance the elongation of a hollow coleoptile in seeds that are seeded directly into shallow paddies. SUBMERGENCE 1 ( SUB1 ), encoding the ethylene‐responsive transcription factor SUB1A‐1 , confers tolerance to complete submergence by dampening carbohydrate catabolism, to enhance recovery upon desubmergence. Interactions between AG1/TPP7 and SUB1/SUB1A‐1 were investigated under three flooding scenarios using four near‐isogenic lines by surveying growth and survival. Pyramiding of the two loci does not negatively affect anaerobic germination or vegetative‐stage submergence tolerance. However, the pyramided AG1 SUB1 genotype displays reduced survival when seeds are planted underwater and maintained under submergence for 16 d. To better understand the roles of TPP7 and SUB1A‐1 and their interaction, temporal changes in carbohydrates and shoot transcriptomes were monitored in the four genotypes varying at the two loci at four developmental timeponts, from day 2 after seeding through day 14 of complete submergence. TPP7 enhances early coleoptile elongation, whereas SUB1A‐1 promotes precocious photoautotrophy and then restricts underwater elongation. By contrast, pyramiding of the AG1 and SUB1 slows elongation growth, the transition to photoautotrophy, and survival. mRNA‐sequencing highlights time‐dependent and genotype‐specific regulation of mRNAs associated with DNA repair, cell cycle, chromatin modification, plastid biogenesis, carbohydrate catabolism and transport, elongation growth, and other processes. These results suggest that interactions between AG1/TPP7 and SUB1/SUB1A‐1 could impact seedling establishment if paddy depth is not effectively managed after direct seeding.

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A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana

Cited by 141 publications

References 60 publications

Eco-Physiological Traits Related to Recovery from Complete Submergence in the Model Legume Lotus japonicus

Eco-Physiological Traits Related to Recovery from Complete Submergence in the Model Legume Lotus japonicus

Hormone dependent survival mechanisms of plants during post-waterlogging stress

Flood resilience loci SUBMERGENCE 1 and ANAEROBIC GERMINATION 1 interact in seedlings established underwater

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