The build-up of osmotic stress responses within the growing root apex using kinematics and RNA-sequencing

Royer, Mathilde; Cohen, David; Aubry, Nathalie; Vendramin, Vera; Scalabrin, Simone; Cattonaro, Federica; Bogeat‐Triboulot, Marie‐Béatrice; Hummel, Irène

doi:10.1093/jxb/erw350

Cited by 12 publications

(15 citation statements)

References 84 publications

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“…Furthermore, a majority of these DAPs were identified only in one of the three treatments. Such proteomic changes agree with previous studies indicating a very small number of proteins and genes overlapped spatially in different root regions under drought stress, and temporally from drought treatment to recovery adjustments phases [40,41].…”

Section: Discussionsupporting

confidence: 92%

Comparative Proteomics of Root Apex and Root Elongation Zones Provides Insights into Molecular Mechanisms for Drought Stress and Recovery Adjustment in Switchgrass

Sangireddy

et al. 2020

Proteomes

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Switchgrass plants were grown in a Sandwich tube system to induce gradual drought stress by withholding watering. After 29 days, the leaf photosynthetic rate decreased significantly, compared to the control plants which were watered regularly. The drought-treated plants recovered to the same leaf water content after three days of re-watering. The root tip (1cm basal fragment, designated as RT1 hereafter) and the elongation/maturation zone (the next upper 1 cm tissue, designated as RT2 hereafter) tissues were collected at the 29th day of drought stress treatment, (named SDT for severe drought treated), after one (D1W) and three days (D3W) of re-watering. The tandem mass tags mass spectrometry-based quantitative proteomics analysis was performed to identify the proteomes, and drought-induced differentially accumulated proteins (DAPs). From RT1 tissues, 6156, 7687, and 7699 proteins were quantified, and 296, 535, and 384 DAPs were identified in the SDT, D1W, and D3W samples, respectively. From RT2 tissues, 7382, 7255, and 6883 proteins were quantified, and 393, 587, and 321 proteins DAPs were identified in the SDT, D1W, and D3W samples. Between RT1 and RT2 tissues, very few DAPs overlapped at SDT, but the number of such proteins increased during the recovery phase. A large number of hydrophilic proteins and stress-responsive proteins were induced during SDT and remained at a higher level during the recovery stages. A large number of DAPs in RT1 tissues maintained the same expression pattern throughout drought treatment and the recovery phases. The DAPs in RT1 tissues were classified in cell proliferation, mitotic cell division, and chromatin modification, and those in RT2 were placed in cell wall remodeling and cell expansion processes. This study provided information pertaining to root zone-specific proteome changes during drought and recover phases, which will allow us to select proteins (genes) as better defined targets for developing drought tolerant plants. The mass spectrometry proteomics data are available via ProteomeXchange with identifier PXD017441.

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Section: Discussionsupporting

confidence: 92%

Comparative Proteomics of Root Apex and Root Elongation Zones Provides Insights into Molecular Mechanisms for Drought Stress and Recovery Adjustment in Switchgrass

Sangireddy

et al. 2020

Proteomes

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“…In the primary root, the altered cellular patterns resulting from root growth under stressful conditions could be a useful experimental subject to approach to further unravel the role of different components on morphogenetic patterns in this organ. For example, under ionic stress conditions in Arabidopsis and under osmotic or water stress in maize, rice, and hybrid poplar, the cell expansion and cell production rate are affected, thus altering primary root growth [60][61][62][63][64][65]. The strength of the osmotic stress also affects each root domain differently, i.e., the meristematic cell number that is reduced in severe stress (−1.2 MPa), affecting the size of the Arabidopsis primary root [41].…”

Section: Discussionmentioning

confidence: 99%

Natural Root Cellular Variation in Responses to Osmotic Stress in Arabidopsis thaliana Accessions

Sánchez

Aceves-García

Fernández-Marcos

et al. 2019

Genes

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Arabidopsis naturally occurring populations have allowed for the identification of considerable genetic variation remodeled by adaptation to different environments and stress conditions. Water is a key resource that limits plant growth, and its availability is initially sensed by root tissues. The root's ability to adjust its physiology and morphology under water deficit makes this organ a useful model to understand how plants respond to water stress. Here, we used hyperosmotic shock stress treatments in different Arabidopsis accessions to analyze the root cell morphological responses. We found that osmotic stress conditions reduced root growth and root apical meristem (RAM) size, promoting premature cell differentiation without affecting the stem cell niche morphology. This phenotype was accompanied by a cluster of small epidermal and cortex cells with radial expansion and root hairs at the transition to the elongation zone. We also found this radial expansion with root hairs when plants are grown under hypoosmotic conditions. Finally, root growth was less affected by osmotic stress in the Sg-2 accession followed by Ws, Cvi-0, and Col-0; however, after a strong osmotic stress, Sg-2 and Cvi-0 were the most resilience accessions. The sensitivity differences among these accessions were not explained by stress-related gene expression. This work provides new cellular insights on the Arabidopsis root phenotypic variability and plasticity to osmotic stress.Genes 2019, 10, 983 2 of 23 northern hemisphere and consequently is subjected to diverse environmental conditions, generating different natural variants called accessions [1]. The Arabidopsis accessions are an important genetic resource to identify mechanisms underlying plant development and stress tolerance as plant genotypes are constantly shaped by biotic and abiotic factors [2]. These phenotypic and genetic variations have enabled the characterization of responses in Arabidopsis natural variants using a range of different approaches [3][4][5][6][7][8].Water deficit is an abiotic stress that affects plant development and productivity. Water availability can be altered by changes in solute concentration (i.e., sugars, salt, inorganic cations and anions) during drought, cold stress, and freezing [9,10]. Some phenotypic and genetic analyses have identified tolerant accessions that can be useful to study the traits related to water deficit tolerance [11,12] (for a review see [13]).Although stress affects the whole organism [14-17], leaves and roots display different responses in order to reduce water loss and promote water foraging for survival [18]. Accordingly, plant roots act on the frontlines by sensing the water deficit, adjusting osmotic homeostasis, forcing water entrance, and avoiding water loss through the accumulation of compatible solutes inside the tissues [19,20]. This rapid root response allows increased water uptake to maintain cellular turgor and reduce the negative effects in the leaves; however, when the stress becomes more severe, the growth in all ...

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“…The second experiment (Exp2) examined the response of the Flevo genotype to different treatments, and was carried out from February to June 2017, using a random design for replication per treatment ( n =3–12 roots). In Exp2, treatments were applied by adding chemicals to the nutrient solution without manipulation of the roots ( Royer et al , 2016 ; Bizet et al , 2017 ). Roots were subjected to either 70 mM NaCl or 160 g l −1 polyethylene glycol (PEG 4000, Merck Chemicals, Darmstadt, Germany), generating osmotic potentials of –0.30 MPa and –0.37 MPa, respectively (measured with a Wescor 5500; Logan, UT, USA).…”

Section: Methodsmentioning

confidence: 99%

“…A better understanding of the mechanisms driving variation in root growth has been obtained by kinematics—a powerful mathematical framework with which to analyse the spatial distribution of growth ( Silk and Erickson, 1979 ; Sharp et al , 1988 , 2004 ; Beemster et al , 2002 ; Walter et al , 2009 ; Royer et al , 2016 ). For instance, the developmental acceleration of root growth has been shown to be accompanied by increased cell production with little change in cell expansion rate ( Beemster and Baskin, 1998 ).…”

Section: Introductionmentioning

confidence: 99%

Quantitative dissection of variations in root growth rate: a matter of cell proliferation or of cell expansion?

Youssef

Bizet

Bastien

et al. 2018

Journal of Experimental Botany

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The build-up of osmotic stress responses within the growing root apex using kinematics and RNA-sequencing

Abstract: HighlightOsmotic stress rapidly induces strong transcriptome responses within the root apex and interferes with growth through a deep remodeling of hormonal status rather than by repressing the machinery of expansive growth.

Cited by 12 publications

References 84 publications

Comparative Proteomics of Root Apex and Root Elongation Zones Provides Insights into Molecular Mechanisms for Drought Stress and Recovery Adjustment in Switchgrass

Comparative Proteomics of Root Apex and Root Elongation Zones Provides Insights into Molecular Mechanisms for Drought Stress and Recovery Adjustment in Switchgrass

Natural Root Cellular Variation in Responses to Osmotic Stress in Arabidopsis thaliana Accessions

Quantitative dissection of variations in root growth rate: a matter of cell proliferation or of cell expansion?

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