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The nature of the progression of drought stress drives differential metabolomic responses in Populus deltoides.

ABSTRACT: BACKGROUND AND AIMS:The use of woody crops for Quad-level (approx. 1 × 1018 J) energy production will require marginal agricultural lands that experience recurrent periods of water stress. Populus species have the capacity to increase dehydration tolerance by lowering osmotic potential via osmotic adjustment. The aim of this study was to investigate how the inherent genetic potential of a Populus clone to respond to drought interacts with the nature of the drought to determine the degree of biochemical response. METHODS:A greenhouse drought stress study was conducted on Populus deltoides 'WV94' and the resulting metabolite profiles of leaves were determined by gas chromatography-mass spectrometry following trimethylsilylation for plants subjected to cyclic mild (-0.5 MPa pre-dawn leaf water potential) drought vs. cyclic severe (-1.26 MPa) drought in contrast to well-watered controls (-0.1 MPa) after two or four drought cycles, and in contrast to plants subjected to acute drought, where plants were desiccated for up to 8 d. KEY RESULTS:The nature of drought (cyclic vs. acute), frequency of drought (number of cycles) and the severity of drought (mild vs. severe) all dictated the degree of osmotic adjustment and the nature of the organic solutes that accumulated. Whereas cyclic drought induced the largest responses in primary metabolism (soluble sugars, organic acids and amino acids), acute onset of prolonged drought induced the greatest osmotic adjustment and largest responses in secondary metabolism, especially populosides (hydroxycinnamic acid conjugates of salicin). CONCLUSIONS:The differential adaptive metabolite responses in cyclic vs. acute drought suggest that stress acclimation occurs via primary metabolism in response to cyclic drought, whereas expanded metabolic plasticity occurs via secondary metabolism following severe, acute drought. The shift in carbon partitioning to aromatic metabolism with the production of a diverse suite of higher order salicylates lowers osmotic potential and increases the probability of post-stress recovery.

SUBMITTER: Tschaplinski TJ

PROVIDER: S-EPMC6821281 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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The nature of the progression of drought stress drives differential metabolomic responses in Populus deltoides.

Tschaplinski Timothy James TJ Abraham Paul E PE Jawdy Sara S SS Gunter Lee E LE Martin Madhavi Z MZ Engle Nancy L NL Yang Xiaohan X Tuskan Gerald A GA

Annals of botany 20191001 4

<h4>Background and aims</h4>The use of woody crops for Quad-level (approx. 1 × 1018 J) energy production will require marginal agricultural lands that experience recurrent periods of water stress. Populus species have the capacity to increase dehydration tolerance by lowering osmotic potential via osmotic adjustment. The aim of this study was to investigate how the inherent genetic potential of a Populus clone to respond to drought interacts with the nature of the drought to determine the degree ...[more]

PMID: 30689716

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Project description:Drought stress is a recurring feature of world climate and the single most important factor influencing agricultural yield worldwide. Plants display highly variable, species-specific responses to drought and these responses are multifaceted, requiring physiological and morphological changes influenced by genetic and molecular mechanisms. Moreover, the reproducibility of water deficit studies is very cumbersome, which significantly impedes research on drought tolerance, because how a plant responds is highly influenced by the timing, duration, and intensity of the water deficit. Despite progress in the identification of drought-related mechanisms in many plants, the molecular basis of drought resistance remains to be fully understood in trees, particularly in poplar species because their wide geographic distribution results in varying tolerances to drought. Herein, we aimed to better understand this complex phenomenon in eastern cottonwood (Populus deltoides) by performing a detailed contrast of the proteome changes between two different water deficit experiments to identify functional intersections and divergences in proteome responses. We investigated plants subjected to cyclic water deficit and compared these responses to plants subjected to prolonged acute water deficit. In total, we identified 108,012 peptide sequences across both experiments that provided insight into the quantitative state of 22,737 Populus gene models and 8,199 functional protein groups in response to drought. Together, these datasets provide the most comprehensive insight into proteome drought responses in poplar to date and a direct proteome comparison between short period dehydration shock and cyclic, post-drought re-watering. Overall, this investigation provides novel insights into drought avoidance mechanisms that are distinct from progressive drought stress. Additionally, we identified proteins that have been associated as drought-relevant in previous studies. Importantly, we highlight the RD26 transcription factor as a gene regulated at both the transcript and protein level, regardless of species and drought condition, and, thus, represents a key, universal drought marker for Populus species.

Project description:BackgroundPoplar trees provide a large amount of wood material, but many parts of the world are arid or semi-arid areas because of insufficient annual precipitation, which seriously affects the growth of poplar trees. Populus simonii 'Tongliao1' shows strong tolerance to stress environments, and Populus deltoides 'Danhong' shows a stronger growth rate in a suitable environment. To identify drought tolerance-related QTLs and genes, an F1 population derived from the cross between the 'Danhong' and 'Tongliao 1' Populus was assessed under drought stress.ResultsWe measured drought-related traits such as the relative height growth, relative diameter growth, leaf senescence number, specific leaf area, and leaf relative water content in the population under control and drought environments. The results showed that drought stress reduced the plant height relative growth, ground diameter relative growth, specific leaf area and leaf relative water content and increased the number of leaf drops. A total of 208 QTLs were identified by QTL mapping analysis, and they consisted of 92, 63 and 53 QTLs under control, drought stress treatment and drought index conditions, respectively. A molecular identification marker for drought tolerance, np2841, which was associated with a QTL (qDLRWC-LG10-1) for relative leaf water content, was initially developed. We mined 187 candidate genes for QTL regions of five traits under a drought environment. The reference genome annotation for Populus trichocarpa and a homologous gene analysis of Arabidopsis thaliana identified two candidate genes, Potri.003G171300 and Potri.012G123900, with significant functions in response to drought stress. We identified five key regulatory genes (Potri.006G273500, Potri.007G111500, Potri.007G111600, Potri.007G111700, and Potri.007G111800) related to drought tolerance through the poplar coexpression network.ConclusionIn this study, our results indicate that the QTLs can effectively enhance the drought tolerance of poplar. It is a step closer towards unravelling the genetic basis of poplar drought tolerance-related traits, and to providing validated candidate genes and molecular markers for future genetic improvement.

Project description:BackgroundNitrogen (N) is one of the main factors limiting the wood yield in poplar cultivation. Understanding the molecular mechanism of N utilization could play a guiding role in improving the nitrogen use efficiency (NUE) of poplar.ResultsIn this study, three N-efficient genotypes (A1-A3) and three N-inefficient genotypes (C1-C3) of Populus deltoides were cultured under low N stress (5 μM NH4NO3) and normal N supply (750 μM NH4NO3). The dry matter mass, leaf morphology, and chlorophyll content of both genotypes decreased under N starvation. The low nitrogen adaptation coefficients of the leaves and stems biomass of group A were significantly higher than those of group C (p < 0.05). Interestingly, N starvation induced fine root growth in group A, but not in group C. Next, a detailed time-course analysis of enzyme activities and gene expression in leaves identified 2062 specifically differentially expressed genes (DEGs) in group A and 1118 in group C. Moreover, the sensitivity to N starvation of group A was weak, and DEGs related to hormone signal transduction and stimulus response played an important role in the low N response this group. Weighted gene co-expression network analysis identified genes related to membranes, catalytic activity, enzymatic activity, and response to stresses that might be critical for poplar's adaption to N starvation and these genes participated in the negative regulation of various biological processes. Finally, ten influential hub genes and twelve transcription factors were identified in the response to N starvation. Among them, four hub genes were related to programmed cell death and the defense response, and PodelWRKY18, with high connectivity, was involved in plant signal transduction. The expression of hub genes increased gradually with the extension of low N stress time, and the expression changes in group A were more obvious than those in group C.ConclusionsUnder N starvation, group A showed stronger adaptability and better NUE than group C in terms of morphology and physiology. The discovery of hub genes and transcription factors might provide new information for the analysis of the molecular mechanism of NUE and its improvement in poplar.

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The nature of the progression of drought stress drives differential metabolomic responses in Populus deltoides.

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The nature of the progression of drought stress drives differential metabolomic responses in Populus deltoides.

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