Insights from transcriptome profiling on the non-photosynthetic and stomatal signaling response of maize carbonic anhydrase mutants to low CO2

Journal Article · Fri Feb 15 00:00:00 EST 2019 · BMC Genomics

DOI:https://doi.org/10.1186/s12864-019-5522-7· OSTI ID:1618571

Kolbe, Allison R. ; Studer, Anthony J.; Cornejo, Omar E.; Cousins, Asaph B.

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 CO₂ concentrations. 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.

• Research Organization: Life Sciences Research Foundation, Princeton, NJ (United States); Donald Danforth Plant Science Center, St. Louis, MO (United States)
• Sponsoring Organization: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA
• Grant/Contract Number: SC0008769; FG02-12ER16337; SC0008510
• OSTI ID: 1618571
• Alternate ID(s): OSTI ID: 1611066
• Journal Information: BMC Genomics, Journal Name: BMC Genomics Vol. 20 Journal Issue: 1; ISSN 1471-2164
• Publisher: Springer
• Country of Publication: United Kingdom
• Language: English

Related Subjects

60 APPLIED LIFE SCIENCES
Biotechnology & Applied Microbiology
Genetics & Heredity
Carbonic anhydrase
C4 photosynthesis
Low CO2
RNA-seq
Stomata
Zea mays