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

Abstract

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.more » 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.« less

Authors:

Kolbe, Allison R. ;

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• Search DOE PAGES for ORCID "0000-0002-9671-6091"

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

Publication Date:

Fri Feb 15 00:00:00 EST 2019

Research Org.:

Life Sciences Research Foundation, Princeton, NJ (United States); Donald Danforth Plant Science Center, St. Louis, MO (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA

OSTI Identifier:

1618571

Alternate Identifier(s):

OSTI ID: 1611066

Grant/Contract Number:  

SC0008769; FG02-12ER16337; SC0008510

Resource Type:

Published Article

Journal Name:

BMC Genomics

Additional Journal Information:

Journal Name: BMC Genomics Journal Volume: 20 Journal Issue: 1; Journal ID: ISSN 1471-2164

Publisher:

Springer

Country of Publication:

United Kingdom

Language:

English

Subject:

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