Underwater CAM photosynthesis elucidated by Isoetes genome

Nolan T Hartwick,David Wickell,Amra Dhabalia Ashok,Hsiao-Pei Yang,Yao-Moan Huang,Todd P Michael,Jan De Vries,Sophie De Vries,Zheng Li,Iker Irisarri,Fay-Wei Li,Li-Yaung Kuo,Michael S Barker,Armin Dadras

doi:10.1038/s41467-021-26644-7

Abstract

To conserve water in arid environments, numerous plant lineages have independently evolved Crassulacean Acid Metabolism (CAM). Interestingly, Isoetes, an aquatic lycophyte, can also perform CAM as an adaptation to low CO2 availability underwater. However, little is known about the evolution of CAM in aquatic plants and the lack of genomic data has hindered comparison between aquatic and terrestrial CAM. Here, we investigate underwater CAM in Isoetes taiwanensis by generating a high-quality genome assembly and RNA-seq time course. Despite broad similarities between CAM in Isoetes and terrestrial angiosperms, we identify several key differences. Notably, Isoetes may have recruited the lesser-known ‘bacterial-type’ PEPC, along with the ‘plant-type’ exclusively used in other CAM and C4 plants for carboxylation of PEP. Furthermore, we find that circadian control of key CAM pathway genes has diverged considerably in Isoetes relative to flowering plants. This suggests the existence of more evolutionary paths to CAM than previously recognized.

Highlights

To conserve water in arid environments, numerous plant lineages have independently evolved Crassulacean Acid Metabolism (CAM)
Underwater, Isoetes can conduct CAM3, a carbon concentrating mechanism involving the separation of carbon uptake and fixation in a time of day (TOD) fashion, with carbon being sequestered as malate at night, to be fed into the Calvin cycle during the day
Subsequent examination of lignin biosynthesis genes in I. taiwanensis suggests that evolution of particular pathway steps to S-lignin likely predates the divergence of Isoetes and Selaginella (Supplementary Note 3 and Supplementary Figs. 5-17)

Summary

Introduction

To conserve water in arid environments, numerous plant lineages have independently evolved Crassulacean Acid Metabolism (CAM). Neither of the other two MDH genes that cycle in I. taiwanensis exhibit similar expression to their orthologues in terrestrial CAM species (Supplementary Fig. 26).

Results

Conclusion