Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO2
Abstract Background Carbonic anhydrase (CA) catalyzes the hydration of CO2 in the first biochemical step of C4 photosynthesis, and has been considered a potentially rate-limiting step when CO2 availability within a leaf is low. Previous work in Zea mays (maize) with a double knockout of the two high...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2019-02-01
|
| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12864-019-5522-7 |
| _version_ | 1811324963201744896 |
|---|---|
| author | Allison R. Kolbe Anthony J. Studer Omar E. Cornejo Asaph B. Cousins |
| author_facet | Allison R. Kolbe Anthony J. Studer Omar E. Cornejo Asaph B. Cousins |
| author_sort | Allison R. Kolbe |
| collection | DOAJ |
| description | Abstract Background Carbonic anhydrase (CA) catalyzes the hydration of CO2 in the first biochemical step of C4 photosynthesis, and has been considered a potentially rate-limiting step when CO2 availability within a leaf is low. Previous work in Zea mays (maize) with a double knockout of the two highest-expressed β-CA genes, CA1 and CA2, reduced total leaf CA activity to less than 3% of wild-type. Surprisingly, this did not limit photosynthesis in maize at ambient or higher CO2concentrations. However, the ca1ca2 mutants exhibited reduced rates of photosynthesis at sub-ambient CO2, and accumulated less biomass when grown under sub-ambient CO2 (9.2 Pa). To further clarify the importance of CA for C4 photosynthesis, we assessed gene expression changes in wild-type, ca1 and ca1ca2 mutants in response to changes in pCO2 from 920 to 9.2 Pa. Results Leaf samples from each genotype were collected for RNA-seq analysis at high CO2 and at two time points after the low CO2 transition, in order to identify early and longer-term responses to CO2 deprivation. Despite the existence of multiple isoforms of CA, no other CA genes were upregulated in CA mutants. Although photosynthetic genes were downregulated in response to low CO2, differential expression was not observed between genotypes. However, multiple indicators of carbon starvation were present in the mutants, including amino acid synthesis, carbohydrate metabolism, and sugar signaling. In particular, multiple genes previously implicated in low carbon stress such as asparagine synthetase, amino acid transporters, trehalose-6-phosphate synthase, as well as many transcription factors, were strongly upregulated. Furthermore, genes in the CO2 stomatal signaling pathway were differentially expressed in the CA mutants under low CO2. Conclusions Using a transcriptomic approach, we showed that carbonic anhydrase mutants do not compensate for the lack of CA activity by upregulating other CA or photosynthetic genes, but rather experienced extreme carbon stress when grown under low CO2. Our results also support a role for CA in the CO2 stomatal signaling pathway. This study provides insight into the importance of CA for C4 photosynthesis and its role in stomatal signaling. |
| first_indexed | 2024-04-13T14:24:42Z |
| format | Article |
| id | doaj.art-fc2c3123b2e045038cf31ca069ef3dc1 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-04-13T14:24:42Z |
| publishDate | 2019-02-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-fc2c3123b2e045038cf31ca069ef3dc12022-12-22T02:43:22ZengBMCBMC Genomics1471-21642019-02-0120111310.1186/s12864-019-5522-7Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO2Allison R. Kolbe0Anthony J. Studer1Omar E. Cornejo2Asaph B. Cousins3School of Biological Sciences, Washington State UniversityDepartment of Crop Sciences, University of Illinois Urbana-ChampaignSchool of Biological Sciences, Washington State UniversitySchool of Biological Sciences, Washington State UniversityAbstract Background Carbonic anhydrase (CA) catalyzes the hydration of CO2 in the first biochemical step of C4 photosynthesis, and has been considered a potentially rate-limiting step when CO2 availability within a leaf is low. Previous work in Zea mays (maize) with a double knockout of the two highest-expressed β-CA genes, CA1 and CA2, reduced total leaf CA activity to less than 3% of wild-type. Surprisingly, this did not limit photosynthesis in maize at ambient or higher CO2concentrations. However, the ca1ca2 mutants exhibited reduced rates of photosynthesis at sub-ambient CO2, and accumulated less biomass when grown under sub-ambient CO2 (9.2 Pa). To further clarify the importance of CA for C4 photosynthesis, we assessed gene expression changes in wild-type, ca1 and ca1ca2 mutants in response to changes in pCO2 from 920 to 9.2 Pa. Results Leaf samples from each genotype were collected for RNA-seq analysis at high CO2 and at two time points after the low CO2 transition, in order to identify early and longer-term responses to CO2 deprivation. Despite the existence of multiple isoforms of CA, no other CA genes were upregulated in CA mutants. Although photosynthetic genes were downregulated in response to low CO2, differential expression was not observed between genotypes. However, multiple indicators of carbon starvation were present in the mutants, including amino acid synthesis, carbohydrate metabolism, and sugar signaling. In particular, multiple genes previously implicated in low carbon stress such as asparagine synthetase, amino acid transporters, trehalose-6-phosphate synthase, as well as many transcription factors, were strongly upregulated. Furthermore, genes in the CO2 stomatal signaling pathway were differentially expressed in the CA mutants under low CO2. Conclusions Using a transcriptomic approach, we showed that carbonic anhydrase mutants do not compensate for the lack of CA activity by upregulating other CA or photosynthetic genes, but rather experienced extreme carbon stress when grown under low CO2. Our results also support a role for CA in the CO2 stomatal signaling pathway. This study provides insight into the importance of CA for C4 photosynthesis and its role in stomatal signaling.http://link.springer.com/article/10.1186/s12864-019-5522-7Carbonic anhydraseC4 photosynthesisLow CO2RNA-seqStomataZea mays |
| spellingShingle | Allison R. Kolbe Anthony J. Studer Omar E. Cornejo Asaph B. Cousins Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO2 BMC Genomics Carbonic anhydrase C4 photosynthesis Low CO2 RNA-seq Stomata Zea mays |
| title | Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO2 |
| title_full | Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO2 |
| title_fullStr | Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO2 |
| title_full_unstemmed | Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO2 |
| title_short | Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO2 |
| title_sort | insights from transcriptome profiling on the non photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low co2 |
| topic | Carbonic anhydrase C4 photosynthesis Low CO2 RNA-seq Stomata Zea mays |
| url | http://link.springer.com/article/10.1186/s12864-019-5522-7 |
| work_keys_str_mv | AT allisonrkolbe insightsfromtranscriptomeprofilingonthenonphotosyntheticandstomatalsignalingresponseofmaizecarbonicanhydrasemutantstolowco2 AT anthonyjstuder insightsfromtranscriptomeprofilingonthenonphotosyntheticandstomatalsignalingresponseofmaizecarbonicanhydrasemutantstolowco2 AT omarecornejo insightsfromtranscriptomeprofilingonthenonphotosyntheticandstomatalsignalingresponseofmaizecarbonicanhydrasemutantstolowco2 AT asaphbcousins insightsfromtranscriptomeprofilingonthenonphotosyntheticandstomatalsignalingresponseofmaizecarbonicanhydrasemutantstolowco2 |