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Distinct transcriptional profiles of ozone stress in soybean (Glycine max) flowers and pods.

Leisner CP, Ming R, Ainsworth EA - BMC Plant Biol. (2014)

Bottom Line: Current ground-level [O3] are estimated to reduce global soybean yields by 6% to 16%.Pod tissues responded to elevated [O3] by increasing expression of xyloglucan endotransglucosylase/hydrolase genes, which may be involved with increased pod dehiscence in elevated [O3].This study established that gene expression in reproductive tissues of soybean are impacted by elevated [O3], and flowers and pods have distinct transcriptomic responses to elevated [O3].

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Biology, University of Illinois, Urbana-Champaign, Urbana, IL, 61801, USA. leisner1@illinois.edu.

ABSTRACT

Background: Tropospheric ozone (O3) is a secondary air pollutant and anthropogenic greenhouse gas. Concentrations of tropospheric O3 ([O3] have more than doubled since the Industrial Revolution, and are high enough to damage plant productivity. Soybean (Glycine max L. Merr.) is the world's most important legume crop and is sensitive to O3. Current ground-level [O3] are estimated to reduce global soybean yields by 6% to 16%. In order to understand transcriptional mechanisms of yield loss in soybean, we examined the transcriptome of soybean flower and pod tissues exposed to elevated [O3] using RNA-Sequencing.

Results: Elevated [O3] elicited a strong transcriptional response in flower and pod tissues, with increased expression of genes involved in signaling in both tissues. Flower tissues also responded to elevated [O3] by increasing expression of genes encoding matrix metalloproteinases (MMPs). MMPs are zinc- and calcium-dependent endopeptidases that have roles in programmed cell death, senescence and stress response in plants. Pod tissues responded to elevated [O3] by increasing expression of xyloglucan endotransglucosylase/hydrolase genes, which may be involved with increased pod dehiscence in elevated [O3].

Conclusions: This study established that gene expression in reproductive tissues of soybean are impacted by elevated [O3], and flowers and pods have distinct transcriptomic responses to elevated [O3].

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Related in: MedlinePlus

Comparison of expression changes in response to elevated [O3] in soybean flowers and pods. The log fold change of the 277 individual genes significantly changing in response to elevated [O3] in both pods vs. flowers is shown. Functional groups are represented by different symbols/colors. The 1:1 line represents genes that have the same direction of fold change in flower and pod tissue.
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Fig5: Comparison of expression changes in response to elevated [O3] in soybean flowers and pods. The log fold change of the 277 individual genes significantly changing in response to elevated [O3] in both pods vs. flowers is shown. Functional groups are represented by different symbols/colors. The 1:1 line represents genes that have the same direction of fold change in flower and pod tissue.

Mentions: Differentially expressed genes in pods and flowers were grouped into functional categories (Figure 4). Nine of 15 total functional categories showed pod and flower genes changing in the same direction in response to elevated [O3] (Figure 4). Transcripts involved in signaling, development, transport, stress, protein and RNA were expressed at greater levels on average in both pods and flowers exposed to elevated [O3] compared to control (Figure 4). While average changes in expression based on functional categories suggests that there was overlap in the transcriptional response of flowers and pods to elevated [O3], investigation of individual genes showed that there was not good correspondence of the direction or magnitude of the response (Figure 5). Less than half of the 277 genes that were significantly affected by elevated [O3] in both flowers and pods responded in a similar direction, with 78 of the 277 genes increasing in both tissues in response to elevated [O3] and 33 decreasing in both tissues in response to elevated [O3] (Figure 5). Many of the transcripts that fell on the 1:1 line in Figure 5 were involved in signaling and RNA processing, including 12 leucine-rich repeat receptor-like kinases (RLKs) and 3 cysteine-rich Domain of Unknown Function 26 (DUF26) RLKs (also known as cysteine-rich receptor-like kinases, CRK). Plant RLKs are transmembrane proteins involved in signal perception and form a large multi-gene family with regulatory roles in development, abiotic and biotic stress responses in plants [40,41]. Recent analysis of the response of Arabidopsis DUF26 RLKs showed that many of the 44 RLKs were specifically up-regulated in response to O3 stress in leaves [42], including DUF26 30 (CRK 26), DUF26 29 (CRK 29) and DUF26 41 (CRK 2), which also had a significant increase in expression in soybean pods and flowers exposed to elevated [O3]. Wraczek et al. [42] found that the general pattern of DUF26 expression responses to O3 was most similar to the transcriptional response to pathogen infection, which like O3 elicits an ROS burst in the apolost. The transcriptional response to O3 however, was very different from expression responses to high light treatments or chemical treatments that increased ROS production in chloroplasts or mitochondria [42]. Thus, it was further suggested that the DUF26 domain, which has a conserved cysteine motif C-8X-C-2X-C, could act as an apolastic ROS sensor [42].Figure 4


Distinct transcriptional profiles of ozone stress in soybean (Glycine max) flowers and pods.

Leisner CP, Ming R, Ainsworth EA - BMC Plant Biol. (2014)

Comparison of expression changes in response to elevated [O3] in soybean flowers and pods. The log fold change of the 277 individual genes significantly changing in response to elevated [O3] in both pods vs. flowers is shown. Functional groups are represented by different symbols/colors. The 1:1 line represents genes that have the same direction of fold change in flower and pod tissue.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4263021&req=5

Fig5: Comparison of expression changes in response to elevated [O3] in soybean flowers and pods. The log fold change of the 277 individual genes significantly changing in response to elevated [O3] in both pods vs. flowers is shown. Functional groups are represented by different symbols/colors. The 1:1 line represents genes that have the same direction of fold change in flower and pod tissue.
Mentions: Differentially expressed genes in pods and flowers were grouped into functional categories (Figure 4). Nine of 15 total functional categories showed pod and flower genes changing in the same direction in response to elevated [O3] (Figure 4). Transcripts involved in signaling, development, transport, stress, protein and RNA were expressed at greater levels on average in both pods and flowers exposed to elevated [O3] compared to control (Figure 4). While average changes in expression based on functional categories suggests that there was overlap in the transcriptional response of flowers and pods to elevated [O3], investigation of individual genes showed that there was not good correspondence of the direction or magnitude of the response (Figure 5). Less than half of the 277 genes that were significantly affected by elevated [O3] in both flowers and pods responded in a similar direction, with 78 of the 277 genes increasing in both tissues in response to elevated [O3] and 33 decreasing in both tissues in response to elevated [O3] (Figure 5). Many of the transcripts that fell on the 1:1 line in Figure 5 were involved in signaling and RNA processing, including 12 leucine-rich repeat receptor-like kinases (RLKs) and 3 cysteine-rich Domain of Unknown Function 26 (DUF26) RLKs (also known as cysteine-rich receptor-like kinases, CRK). Plant RLKs are transmembrane proteins involved in signal perception and form a large multi-gene family with regulatory roles in development, abiotic and biotic stress responses in plants [40,41]. Recent analysis of the response of Arabidopsis DUF26 RLKs showed that many of the 44 RLKs were specifically up-regulated in response to O3 stress in leaves [42], including DUF26 30 (CRK 26), DUF26 29 (CRK 29) and DUF26 41 (CRK 2), which also had a significant increase in expression in soybean pods and flowers exposed to elevated [O3]. Wraczek et al. [42] found that the general pattern of DUF26 expression responses to O3 was most similar to the transcriptional response to pathogen infection, which like O3 elicits an ROS burst in the apolost. The transcriptional response to O3 however, was very different from expression responses to high light treatments or chemical treatments that increased ROS production in chloroplasts or mitochondria [42]. Thus, it was further suggested that the DUF26 domain, which has a conserved cysteine motif C-8X-C-2X-C, could act as an apolastic ROS sensor [42].Figure 4

Bottom Line: Current ground-level [O3] are estimated to reduce global soybean yields by 6% to 16%.Pod tissues responded to elevated [O3] by increasing expression of xyloglucan endotransglucosylase/hydrolase genes, which may be involved with increased pod dehiscence in elevated [O3].This study established that gene expression in reproductive tissues of soybean are impacted by elevated [O3], and flowers and pods have distinct transcriptomic responses to elevated [O3].

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Biology, University of Illinois, Urbana-Champaign, Urbana, IL, 61801, USA. leisner1@illinois.edu.

ABSTRACT

Background: Tropospheric ozone (O3) is a secondary air pollutant and anthropogenic greenhouse gas. Concentrations of tropospheric O3 ([O3] have more than doubled since the Industrial Revolution, and are high enough to damage plant productivity. Soybean (Glycine max L. Merr.) is the world's most important legume crop and is sensitive to O3. Current ground-level [O3] are estimated to reduce global soybean yields by 6% to 16%. In order to understand transcriptional mechanisms of yield loss in soybean, we examined the transcriptome of soybean flower and pod tissues exposed to elevated [O3] using RNA-Sequencing.

Results: Elevated [O3] elicited a strong transcriptional response in flower and pod tissues, with increased expression of genes involved in signaling in both tissues. Flower tissues also responded to elevated [O3] by increasing expression of genes encoding matrix metalloproteinases (MMPs). MMPs are zinc- and calcium-dependent endopeptidases that have roles in programmed cell death, senescence and stress response in plants. Pod tissues responded to elevated [O3] by increasing expression of xyloglucan endotransglucosylase/hydrolase genes, which may be involved with increased pod dehiscence in elevated [O3].

Conclusions: This study established that gene expression in reproductive tissues of soybean are impacted by elevated [O3], and flowers and pods have distinct transcriptomic responses to elevated [O3].

Show MeSH
Related in: MedlinePlus