Arabidopsis plants expressing only the redox‐regulated Rca‐α isoform have constrained photosynthesis and plant growth

• Published in: The Plant journal : for cell and molecular biology 2020-09, Vol.103 (6), p.2250-2262
• Main Authors: Kim, Sang Yeol, Stessman, Dan J., Wright, David A., Spalding, Martin H., Huber, Steven C., Ort, Donald R.
• Format: Article
• Language: English
• Subjects: Activation; Alternative splicing; Arabidopsis; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis - physiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Assimilation; BASIC BIOLOGICAL SCIENCES; Carbon dioxide; Energy crops; Flowers & plants; Gene Expression Regulation, Plant; Isoforms; Light; Light intensity; Luminous intensity; Oligomers; Oxidation-Reduction; Phenotype; Photosynthesis; Plant growth; Plant species; Plants, Genetically Modified; Protein Isoforms; Ribulose-bisphosphate carboxylase; Rubisco; rubisco activase; Species; Splicing; Transgenic plants
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.14897

SUMMARY Rubisco activase (Rca) facilitates the release of sugar‐phosphate inhibitors from the active sites of Rubisco and thereby plays a central role in initiating and sustaining Rubisco activation. In Arabidopsis, alternative splicing of a single Rca gene results in two Rca isoforms, Rca‐α and Rca‐β. Redox modulation of Rca‐α regulates the function of Rca‐α and Rca‐β acting together to control Rubisco activation. Although Arabidopsis Rca‐α alone less effectively activates Rubisco in vitro, it is not known how CO2 assimilation and plant growth are impacted. Here, we show that two independent transgenic Arabidopsis lines expressing Rca‐α in the absence of Rca‐β (‘Rca‐α only’ lines) grew more slowly in various light conditions, especially under low light or fluctuating light intensity, and in a short day photoperiod compared to wildtype. Photosynthetic induction was slower in the Rca‐α only lines, and they maintained a lower rate of CO2 assimilation during both photoperiod types. Our findings suggest Rca oligomers composed of Rca‐α only are less effective in initiating and sustaining the activation of Rubisco than when Rca‐β is also present. Currently there are no examples of any plant species that naturally express Rca‐α only but numerous examples of species expressing Rca‐β only. That Rca‐α exists in most plant species, including many C3 and C4 food and bioenergy crops, implies its presence is adaptive under some circumstances. Significance Statement Alternative splicing of a single Arabidopsis Rubisco activase (Rca) gene yields two Rca isoforms, Rca‐α and Rca‐β, and we show Rca‐α only expression less effectively regulates Rubisco and reduces Arabidopsis plant growth and photosynthesis compared to the presence of both isoforms or Rca‐β only expression. A search of genomic databases revealed no plant species that contain only Rca‐α genes, indicating that, when present, Rca‐α must interact with Rca‐β to effectively sustain Rubisco activation.