The ubiquity and coexistence of two FBPases in chloroplasts of photosynthetic eukaryotes and its evolutionary and functional implications

Yujin Li; Qingqing Ye; De He; Huixian Bai; Jianfan Wen

doi:10.1016/j.pld.2019.09.002

The ubiquity and coexistence of two FBPases in chloroplasts of photosynthetic eukaryotes and its evolutionary and functional implications

Plant Divers. 2019 Sep 26;42(2):120-125. doi: 10.1016/j.pld.2019.09.002. eCollection 2020 Apr.

Authors

Yujin Li^{1

2}, Qingqing Ye¹, De He³, Huixian Bai¹, Jianfan Wen¹

Affiliations

¹ State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, 650223, China.
² Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan, 650204, China.
³ College of Life Sciences, Southwest Forestry University, Kunming, Yunnan, 650224, China.

Abstract

In photosynthetic eukaryotes, there are two well-characterized fructose-1,6-bisphosphatases (FBPases): the redox-insensitive cytosolic FBPase (cyFBPase), which participates in gluconeogenesis, and the redox-sensitive chloroplastic FBPase (cpFBPase1), which is a critical enzyme in the Calvin cycle. Recent studies have identified a new chloroplastic FBPase, cpFBPase2; however, its phylogenetic distribution, evolutionary origin, and physiological function remain unclear. In this study, we identified and characterized these three FBPase isoforms in diverse, representative photosynthetic lineages and analyzed their phylogeny. In contrast to previous hypotheses, we found that cpFBPase2 is ubiquitous in photosynthetic eukaryotes. Additionally, all cpFBPase2s from diverse lineages form a monophyly, suggesting cpFBPase2 is not a recently evolved enzyme restricted to land plants but rather evolved early in the evolution of photosynthetic organisms, and most likely, in the common ancestor of photosynthetic eukaryotes. cyFBPase was probably first duplicated to produce cpFBPase2, and then the latter duplicated to produce cpFBPase1. The ubiquitous coexistence of these two cpFBPases in chloroplasts is most likely the consequence of adaptation to different redox conditions of photosynthesis, especially those caused by recurrent changes in light conditions.

Keywords: Adaptation; Coexistence; Evolution; FBPase; Photosynthetic eukaryotes.