Early mannitol-triggered changes in the Arabidopsis leaf (phospho)proteome reveal growth regulators

Nikonorova, Natalia; Broeck, Lisa Van den; Zhu, Shanshuo; Cotte, Brigitte van de; Dubois, Marieke; Gevaert, Kris; Inzé, Dirk; Smet, Ive De

doi:10.1093/jxb/ery261

Cited by 40 publications

(34 citation statements)

References 77 publications

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“…Unfortunately, the latter studies lack organ-level resolution necessary to draw conclusions about the timing at which these phosphoproteome changes occur in the shoot. Specifically in shoots, transcriptomics and proteomics analyses found notable osmotic stress-induced changes within 30~60 minutes following osmotic stress (Skirycz et al, 2011a;Nikonorova et al, 2018). Overall, these studies situate the short-term stress response in aerial plant tissues of Arabidopsis around 10~60 minutes upon stress sensing by the roots.…”

Section: Within the First Hour Leaves Close Stomata And Initiate Gromentioning

confidence: 68%

“…In young Arabidopsis leaves, 57 transcripts respond within 1.5 h of stress, or even earlier (Skirycz et al, 2011a;Dubois et al, 2015;Nikonorova et al, 2018). The majority of these genes is involved in ethylene response and, consistently, osmotic stress was shown to trigger an increase in ACC levels in young seedlings after 1 h (Fig.…”

Section: Within the First Hour Leaves Close Stomata And Initiate Gromentioning

confidence: 84%

“…1r) (Yuan et al, 2014). At the molecular level, differential phosphorylation of ~70 proteins was measured in leaves within 30 minutes upon mild mannitol-induced stress (Nikonorova et al, 2018). Other phosphoproteomics studies detected extensive differential phosphorylation upon shorter stress exposure (up to 5 minutes), or investigated phosphoproteome changes by using other osmotic stress compounds, which helped to characterize important stressresponsive phosphorylation pathways, such as the PP2C-SnRK2 described below (Xue et al, 2013;Stecker et al, 2014;Bhaskara et al, 2017a;Wong et al, 2019).…”

Section: Within the First Hour Leaves Close Stomata And Initiate Gromentioning

confidence: 99%

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Plant growth under suboptimal water conditions: early responses and methods to study them

Dubois

Inzé

2020

Journal of Experimental Botany

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Drought stress forms a major environmental constraint during the life cycle of plants, often decreasing plant yield and in extreme cases threatening survival. The molecular and physiological responses induced by drought have been the topic of extensive research during the past decades. Because soil-based approaches to studying drought responses are often challenging due to low throughput and insufficient control of the conditions, osmotic stress assays in plates were developed to mimic drought. Addition of compounds such as polyethylene glycol, mannitol, sorbitol, or NaCl to controlled growth media has become increasingly popular since it offers the advantage of accurate control of stress level and onset. These osmotic stress assays enabled the discovery of very early stress responses, occurring within seconds or minutes following osmotic stress exposure. In this review, we construct a detailed timeline of early responses to osmotic stress, with a focus on how they initiate plant growth arrest. We further discuss the specific responses triggered by different types and severities of osmotic stress. Finally, we compare short-term plant responses under osmotic stress versus in-soil drought and discuss the advantages, disadvantages, and future of these plate-based proxies for drought.

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Section: Within the First Hour Leaves Close Stomata And Initiate Gromentioning

confidence: 68%

Section: Within the First Hour Leaves Close Stomata And Initiate Gromentioning

confidence: 84%

Section: Within the First Hour Leaves Close Stomata And Initiate Gromentioning

confidence: 99%

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Plant growth under suboptimal water conditions: early responses and methods to study them

Dubois

Inzé

2020

Journal of Experimental Botany

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“…Protein phosphorylation has been reported as one of the early posttranslational responses to osmotic stress (Nikonorova et al, 2018), and QSK1 has multiple phosphorylation sites and is phosphorylated in response to abiotic stress (Niittylä et al, 2007;Chang et al, 2012). Using phosphomutants of QSK1, we showed that the phosphorylation status of QSK1 is important for subcellular localization with the QSK1-S621D,S626D-GFP phosphomimic mutant partially associating with plasmodesmata even in control conditions, while the QSK1-S621A,S626A-GFP phosphodead mutant was significantly affected in its capacity to localize to plasmodesmata after mannitol treatment.…”

Section: Discussionmentioning

confidence: 99%

Plasma Membrane-Associated Receptor-like Kinases Relocalize to Plasmodesmata in Response to Osmotic Stress

et al. 2019

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Plasmodesmata act as key elements in intercellular communication, coordinating processes related to plant growth, development, and responses to environmental stresses. While many of the developmental, biotic, and abiotic signals are primarily perceived at the plasma membrane (PM) by receptor proteins, plasmodesmata also cluster receptor-like activities; whether these two pathways interact is currently unknown. Here, we show that specific PM-located Leu-rich-repeat receptor-like-kinases, Qi an Sh ou kinase (QSK1) and inflorescence meristem kinase2, which under optimal growth conditions are absent from plasmodesmata, rapidly relocate and cluster to the pores in response to osmotic stress. This process is remarkably fast, is not a general feature of PM-associated proteins, and is independent of sterol and sphingolipid membrane composition. Focusing on QSK1, previously reported to be involved in stress responses, we show that relocalization in response to mannitol depends on QSK1 phosphorylation. Loss-of-function mutation in QSK1 results in delayed lateral root (LR) development, and the mutant is affected in the root response to mannitol stress. Callosemediated plasmodesmata regulation is known to regulate LR development. We found that callose levels are reduced in the qsk1 mutant background with a root phenotype resembling ectopic expression of PdBG1, an enzyme that degrades callose at the pores. Both the LR and callose phenotypes can be complemented by expression of wild-type and phosphomimic QSK1 variants, but not by phosphodead QSK1 mutant, which fails to relocalize at plasmodesmata. Together, the data indicate that reorganization of receptor-like-kinases to plasmodesmata is important for the regulation of callose and LR development as part of the plant response to osmotic stress.

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“…A reduced group of these SnRK3 sequences could be considered founder as were close in the sequence tree to microalgae SnRK3/CKIN3 (Figure 1). Interestingly, between the plant sequences included in this group are Arabidopsis SnRK3.11 or SOS2, a salt stress responsive kinase within the SOS pathway [33], osmostress-sensitive SnRK3.13 [35] and P. pinaster PpiSnRK3.3 and PpiSnRK3.4. This closeness points at once to the ancient (microalgae) origin of this pathway and by analogy to the possible involvement of both microalgae and P. pinaster PpiSnRK3.3 and PpiSnRK3.4 into salt and/or osmotic stress responses.…”

Section: Discussionmentioning

confidence: 99%

The Analysis of Pinus pinaster SnRKs Reveals Clues of the Evolution of This Family and a New Set of Abiotic Stress Resistance Biomarkers

et al. 2020

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Climate change is increasing the intensity and incidence of environmental stressors, reducing the biomass yields of forestry species as Pinus pinaster. Selection of new stress-tolerant varieties is thus required. Many genes related to plant stress signaling pathways have proven useful for this purpose with sucrose non-fermenting related kinases (SnRK), conserved across plant evolution and connected to different phosphorylation cascades within ABA- and Ca2+-mediated signaling pathways, as a good example. The modulation of SnRKs and/or the selection of specific SnRK alleles have proven successful strategies to increase plant stress resistance. Despite this, SnRKs have been barely studied in gymnosperms. In this work P. pinaster SnRK sequences (PpiSnRK) were identified through a homology- and domain-based sequence analysis using Arabidopsis SnRK sequences as query. Moreover, PpiSnRKs links to the gymnosperm stress response were modeled out of the known interactions of PpiSnRKs orthologs from other species with different signaling complexity. This approach successfully identified the pine SnRK family and predicted their central role into the gymnosperm stress response, linking them to ABA, Ca2+, sugar/energy and possibly ethylene signaling. These links made the gymnosperm kinases promising candidates into the search for new stress resistance-related biomarkers, which would be useful into future breeding strategies.

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Early mannitol-triggered changes in the Arabidopsis leaf (phospho)proteome reveal growth regulators

Abstract: We captured early changes in the Arabidopsis thaliana growing leaf proteome and phosphoproteome upon mild mannitol stress and pinpointed novel regulators of shoot growth.

Cited by 40 publications

References 77 publications

Plant growth under suboptimal water conditions: early responses and methods to study them

Plant growth under suboptimal water conditions: early responses and methods to study them

Plasma Membrane-Associated Receptor-like Kinases Relocalize to Plasmodesmata in Response to Osmotic Stress

The Analysis of Pinus pinaster SnRKs Reveals Clues of the Evolution of This Family and a New Set of Abiotic Stress Resistance Biomarkers

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