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. 2021 Nov 23;22(23):12615.
doi: 10.3390/ijms222312615.

Sandbur Drought Tolerance Reflects Phenotypic Plasticity Based on the Accumulation of Sugars, Lipids, and Flavonoid Intermediates and the Scavenging of Reactive Oxygen Species in the Root

Zhiyuan Yang  1   2 , Chao Bai  1   3 , Peng Wang  2   4 , Weidong Fu  1 , Le Wang  2 , Zhen Song  1 , Xin Xi  5 , Hanwen Wu  6 , Guoliang Zhang  1 , Jiahe Wu  2
Affiliations

Sandbur Drought Tolerance Reflects Phenotypic Plasticity Based on the Accumulation of Sugars, Lipids, and Flavonoid Intermediates and the Scavenging of Reactive Oxygen Species in the Root

Zhiyuan Yang et al. Int J Mol Sci. .

Abstract

The perennial grass Cenchrus spinifex (common sandbur) is an invasive species that grows in arid and semi-arid regions due to its remarkable phenotypic plasticity, which confers the ability to withstand drought and other forms of abiotic stress. Exploring the molecular mechanisms of drought tolerance in common sandbur could lead to the development of new strategies for the protection of natural and agricultural environments from this weed. To determine the molecular basis of drought tolerance in C. spinifex, we used isobaric tags for relative and absolute quantitation (iTRAQ) to identify proteins differing in abundance between roots growing in normal soil and roots subjected to moderate or severe drought stress. The analysis of these proteins revealed that drought tolerance in C. spinifex primarily reflects the modulation of core physiological activities such as protein synthesis, transport and energy utilization as well as the accumulation of flavonoid intermediates and the scavenging of reactive oxygen species. Accordingly, plants subjected to drought stress accumulated sucrose, fatty acids, and ascorbate, shifted their redox potential (as determined by the NADH/NAD ratio), accumulated flavonoid intermediates at the expense of anthocyanins and lignin, and produced less actin, indicating fundamental reorganization of the cytoskeleton. Our results show that C. spinifex responds to drought stress by coordinating multiple metabolic pathways along with other adaptations. It is likely that the underlying metabolic plasticity of this species plays a key role in its invasive success, particularly in semi-arid and arid environments.

Keywords: Cenchrus spinifex Cav.; antioxidant; drought; flavonoids; phenotypic plasticity; reactive oxygen species.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Morphological and physiological characteristics of C. spinifex grown under severe drought or normal conditions. (A) Morphology of C. spinifex plants grown under severe drought (G2, 5% soil moisture) and normal (G0, 20% soil moisture) conditions. (B) Comparison of root/shoot ratio. (C) Comparison of the number of tillers. (D) Comparison of the whole life cycle from germination to seed harvesting. (E) Comparison of water use efficiency (WUE). (F) Comparison of carbon to nitrogen (C/N) ratio. Different superscript letters indicate statistically significant (p < 0.05) differences between G0 and G2 conditions based on the Student’s t-test. Differences and standard deviations (error bars) were calculated from the results of three biological replicates. Scale bar = 1 cm.
Figure 2
Figure 2
Proteomic analysis of C. spinifex roots in response to drought stress. (A) The number of unique peptides from the iTRAQ dataset. (B) The distribution of peptide lengths. (C) The percentage of protein sequence coverage. (D) Venn diagrams of the distribution of proteins differing in abundance between the three groups of samples. G0 indicates plants grown under normal conditions (20% soil moisture), G1 indicates plants grown under moderate drought conditions (10% soil moisture), and G2 indicates plants grown under severe drought conditions (5% soil moisture).
Figure 3
Figure 3
Heat map visualization and clustering of DAP expression profiles in C. spinifex roots in response to drought stress. (a) The 385 DAPs formed six clusters based on functional annotations (black = no difference to G0 control group, red = upregulation, green = downregulation). (b) The functional classification of all the identified proteins (red) and DAPs (yellow) based on Gene Ontology terms. (c) The numbers of upregulated and downregulated DAPs in six major functional clusters plus one cluster for other functions and one for non-annotated proteins (green = G1/G0 comparison, red = G2/G0 comparison).
Figure 4
Figure 4
Protein synthesis and transporter functions in C. spinifex roots enhance drought tolerance. (a) Heat map of protein synthesis and transporter proteins. (b) Upper panel: Expression of nine candidate genes encoding DAPs (seven ribosomal proteins, a translational initiation factor and an ABC transporter) analyzed by real-time PCR. Data are means ± standard deviations (n = 3). Different superscript letters indicate statistically significant (p < 0.05) differences between G1 vs. G0 or G2 vs. G0 based on the Student’s t-test. Lower panel: The differential abundance of corresponding DAPs in C. spinifex roots in response to drought stress.
Figure 5
Figure 5
Drought-induced DAPs participate in the biosynthesis of sugars and fatty acids. (a) Heat map of DAPs related to energy metabolism. (b) Sugar content in the G0 control, G1 and G2 groups. (c) Fatty acid biosynthesis pathway. (d) Fatty acid content (five different examples) in the control (green), G1 (orange), and G2 (red) groups. The content of each sugar and fatty acid was measured in triplicate, and the data are means ± standard deviations. Different superscript letters indicate significant differences (p < 0.05) between the drought treatments and control. DW = dry weight. FW = fresh weight.
Figure 6
Figure 6
Secondary metabolic pathways involved in C. spinifex drought tolerance. (a) Heat map visualization of DAPs involved in secondary metabolism. (b) Phenylpropanoid, flavonoid, anthocyanin, and lignin pathways, with red indicating enzymes that are upregulated and green indicating those that are downregulated in response to drought stress. (c) Anthocyanin content of the control group (G0) and drought treatment groups (G1 and G2). (d) Lignin content of the control group (G0) and drought treatment groups (G1 and G2). Anthocyanin and lignin levels are means ± standard deviations of three replicate measurements per group. Different superscript letters indicate a significant difference (p < 0.05) between the treatment and control. DW = dry weight. FW = fresh weight.
Figure 7
Figure 7
Protein landscape of the ASC–GSH cycle in C. spinifex. (a) Heat map visualization of DAPs involved in ROS scavenging in response to drought stress. (b) The ASC-GSH cycle. (c) Ascorbate content of control roots (G0) and those subjected to drought treatment (G1 and G2). (d) Upper panel: NADH quantification. Lower panel: The ratio of NADH and NAD+. The small images show colorimetric reactions for NADH quantification corresponding to the bars below. Data are means ± standard deviations (n = 3). Different superscript letters indicate significant differences between the treatments and the control (p < 0.05). Abbreviations: ASC = ascorbate, DHA = dehydroascorbate, MDA = monodehydroascorbate, GR = glutathione reductase, GSH = glutathione, GSSG = oxidized glutathione, GST = glutathione S-transferase. FW = fresh weight.
Figure 8
Figure 8
Distribution of F-actin in C. spinifex root tip cells under drought stress conditions compared to unstressed controls. (a) Heat map visualization of DAPs involved in the cytoskeleton. (b) F-actin regulates the internalization and formation of phagosomes and the actin cytoskeleton. (c) Abundance of F-actin based on ELISA results and proteomic data. (d) Root tip cells stained with phalloidin, showing the distribution of F-actin (scale bar = 10 μm).
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References

    1. Syamaladevi D.P., Meena S.S., Nagar R.P. Molecular understandings on ‘the never thirsty’ and apomictic Cenchrus grass. Biotechnol. Lett. 2016;38:369–376. doi: 10.1007/s10529-015-2004-0. - DOI - PubMed
    1. Zhang G.L., Zhu Y., Fu W.D., Wang P., Zhang R.H., Zhang Y.L., Song Z., Xia G.-X., Wu J.H. iTRAQ Protein Profile Differential Analysis of Dormant and Germinated Grassbur Twin Seeds Reveals that Ribosomal Synthesis and Carbohydrate Metabolism Promote Germination Possibly Through the PI3K Pathway. Plant Cell Physiol. 2016;57:1244–1256. doi: 10.1093/pcp/pcw074. - DOI - PubMed
    1. Seastedt T.R. Biological control of invasive plant species: A reassessment for the Anthropocene. New Phytol. 2015;205:490–502. doi: 10.1111/nph.13065. - DOI - PubMed
    1. Gao L., Geng Y., Li B., Chen J., Yang J. Genome-wide DNA methylation alterations of Alternanthera philoxeroides in natural and manipulated habitats: Implications for epigenetic regulation of rapid responses to environmental fluctuation and phenotypic variation. Plant Cell Environ. 2010;33:1820–1827. doi: 10.1111/j.1365-3040.2010.02186.x. - DOI - PubMed
    1. Harb A., Krishnan A., Ambavaram M.M.R., Pereira A. Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol. 2010;154:1254–1271. doi: 10.1104/pp.110.161752. - DOI - PMC - PubMed