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Label-Free Quantitative Proteome Analysis Reveals the Underlying Mechanisms of Grain Nuclear Proteins Involved in Wheat Water-Deficit Response

ABSTRACT: In this study, we performed the first nuclear proteome analysis of wheat developing grains under water deficit by using a label-free based quantitative proteomic approach. In total, we identified 625 unique proteins as differentially accumulated proteins (DAPs), of which 398 DAPs were predicted to be localized in nucleus. Under water deficit, 146 DAPs were up-regulated and mainly involved in the stress response and oxidation-reduction process, while 252 were down-regulated and mainly participated in translation, the cellular amino metabolic process, and the oxidation-reduction process. The cis-acting elements analysis of the key nuclear DAPs encoding genes demonstrated that most of these genes contained the same cis-acting elements in the promoter region, mainly including ABRE involved in abscisic acid response, antioxidant response element, MYB responsive to drought regulation and MYC responsive to early drought. The cis-acting elements related to environmental stress and hormones response were relatively abundant. The transcription expression profiling of the nuclear up-regulated DAPs encoding genes under different organs, developmental stages and abiotic stresses was further detected by RNA-seq and Real-time quantitative polymerase chain reaction, and more than 50% of these genes showed consistency between transcription and translation expression. Finally, we proposed a putative synergistic responsive network of wheat nuclear proteome to water deficit, revealing the underlying mechanisms of wheat grain nuclear proteome in response to water deficit.

SUBMITTER: Li T

PROVIDER: S-EPMC8572964 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: Wheat (Triticum aestivum L.) is an economically important grain crop. Two-dimensional gel-based approaches are limited by the low identification rate of proteins and lack of accurate protein quantitation. The recently developed isobaric tag for relative and absolute quantitation (iTRAQ) method allows sensitive and accurate protein quantification. Here, we performed the first iTRAQ-based quantitative proteome and phosphorylated proteins analyses during wheat grain development. RESULTS: The proteome profiles and phosphoprotein characterization of the metabolic proteins during grain development of the elite Chinese bread wheat cultivar Yanyou 361 were studied using the iTRAQ-based quantitative proteome approach, TiO2 microcolumns, and liquid chromatography-tandem mass spectrometry (LC-MS/MS). Among 1,146 non-redundant proteins identified, 421 showed at least 2-fold differences in abundance, and they were identified as differentially expressed proteins (DEPs), including 256 upregulated and 165 downregulated proteins. Of the 421 DEPs, six protein expression patterns were identified, most of which were up, down, and up-down expression patterns. The 421 DEPs were classified into nine functional categories mainly involved in different metabolic processes and located in the membrane and cytoplasm. Hierarchical clustering analysis indicated that the DEPs involved in starch biosynthesis, storage proteins, and defense/stress-related proteins significantly accumulated at the late grain development stages, while those related to protein synthesis/assembly/degradation and photosynthesis showed an opposite expression model during grain development. Quantitative real-time polymerase chain reaction (qRT-PCR) analysis of 12 representative genes encoding different metabolic proteins showed certain transcriptional and translational expression differences during grain development. Phosphorylated proteins analyses demonstrated that 23 DEPs such as AGPase, sucrose synthase, Hsp90, and serpins were phosphorylated in the developing grains and were mainly involved in starch biosynthesis and stress/defense. CONCLUSIONS: Our results revealed a complex quantitative proteome and phosphorylation profile during wheat grain development. Numerous DEPs are involved in grain starch and protein syntheses as well as adverse defense, which set an important basis for wheat yield and quality. Particularly, some key DEPs involved in starch biosynthesis and stress/defense were phosphorylated, suggesting their roles in wheat grain development.

Project description:BackgroundWheat (Triticum aestivum L.) serves as important grain crop widely cultivated in the world, which is often suffered by drought stress in natural conditions. As one of the most important post translation modifications, protein phosphorylation widely participates in plant abiotic stress regulation. In this study, we performed the first comparative analysis of phosphorylated protein characterization in flag leaves and developing grains of elite Chinese bread wheat cultivar Zhongmai 175 under water deficit by combining with proteomic approach and Pro-Q Diamond gel staining.ResultsField experiment showed that water deficit caused significant reduction of plant height, tiller number, ear length and grain yield. 2-DE and Pro-Q Diamond gel staining analysis showed that 58 proteins were phosphorylated among 112 differentially accumulated proteins in response to water deficit, including 20 in the flag leaves and 38 in the developing grains. The phosphorylated proteins from flag leaves mainly involved in photosynthesis, carbohydrate and energy metabolism, while those from developing grains were closely related with detoxification and defense, protein, carbohydrate and energy metabolism. Particularly, water deficit resulted in significant downregulation of phosphorylated modification level in the flag leaves, which could affect photosynthesis and grain yield. However, some important phosphorylated proteins involved in stress defense, energy metabolism and starch biosynthesis were upregulated under water deficit, which could benefit drought tolerance, accelerate grain filling and shorten grain developing time.ConclusionsThe modification level of those identified proteins from flag leaves and grains had great changes when wheat was suffered from water deficit, indicating that phosphoproteins played a key role in response to drought stress. Our results provide new insights into the molecular mechanisms how phosphoproteins respond to drought stress and thus reduce production.

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.

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Label-Free Quantitative Proteome Analysis Reveals the Underlying Mechanisms of Grain Nuclear Proteins Involved in Wheat Water-Deficit Response

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