Genomic and Transcriptomic Insights into the Evolution of C4 Photosynthesis in Grasses

Haomin Lyu; Won Cheol Yim; Qingyi Yu

doi:10.1093/gbe/evae163

journal article Jul 27, 2024

Genomic and Transcriptomic Insights into the Evolution of C4 Photosynthesis in Grasses

Haomin Lyu

Won Cheol Yim

Qingyi Yu

Genome Biology and Evolution Vol. 16 No. 8 · Oxford University Press (OUP)

View at Publisher Save 10.1093/gbe/evae163

Abstract

Abstract
C4 photosynthesis has independently evolved over 62 times within 19 angiosperm families. The recurrent evolution of C4 photosynthesis appears to contradict the complex anatomical and biochemical modifications required for the transition from C3 to C4 photosynthesis. In this study, we conducted an integrated analysis of genomics and transcriptomics to elucidate the molecular underpinnings of convergent C4 evolution in the grass family. Our genome-wide exploration of C4-related gene families suggests that the expansion of these gene families may have played an important role in facilitating C4 evolution in the grass family. A phylogenomic synteny network analysis uncovered the emergence of C4 genes in various C4 grass lineages from a common ancestral gene pool. Moreover, through a comparison between non-C4 and C4 PEPCs, we pinpointed 14 amino acid sites exhibiting parallel adaptations. These adaptations, occurring post the BEP–PACMAD divergence, shed light on why all C4 origins in grasses are confined to the PACMAD clade. Furthermore, our study revealed that the ancestor of Chloridoideae grasses possessed a more favorable molecular preadaptation for C4 functions compared to the ancestor of Panicoideae grasses. This molecular preadaptation potentially explains why C4 photosynthesis evolved earlier in Chloridoideae than in Panicoideae and why the C3-to-C4 transition occurred once in Chloridoideae but multiple times in Panicoideae. Additionally, we found that C4 genes share similar cis-elements across independent C4 lineages. Notably, NAD-ME subtype grasses may have retained the ancestral regulatory machinery of the C4 NADP-ME gene, while NADP-ME subtype grasses might have undergone unique cis-element modifications.

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Details

Published: Jul 27, 2024
Vol/Issue: 16(8)

Authors

H

Haomin Lyu

Tropical Plant Genetic Resources and Disease Research Unit, Daniel K Inouye U.S. Pacific Basin Agricultural Research Center, Agricultural Research Service, U.S. Department of Agriculture , Hilo, HI 96720 , USA; Hawaii Agriculture Research Center , Kunia, HI 96759 , USA

W

Won Cheol Yim

Department of Biochemistry and Molecular Biology, University of Nevada , Reno, NV 89557 , USA

Q

Qingyi Yu

Tropical Plant Genetic Resources and Disease Research Unit, Daniel K Inouye U.S. Pacific Basin Agricultural Research Center, Agricultural Research Service, U.S. Department of Agriculture , Hilo, HI 96720 , USA

Funding

National Institute of Food and Agriculture

Specialty Crop Research Initiative Award: 2019-51181-30472

Cite This Article

Haomin Lyu, Won Cheol Yim, Qingyi Yu (2024). Genomic and Transcriptomic Insights into the Evolution of C4 Photosynthesis in Grasses. Genome Biology and Evolution, 16(8). https://doi.org/10.1093/gbe/evae163

Genomic and Transcriptomic Insights into the Evolution of C4 Photosynthesis in Grasses

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