In-silico, evolutionary, and functional analysis of CHUP1 and its related proteins in Bienertia sinuspersici-a comparative study across C3, C4, CAM, and SCC4 model plants

So Youn Won; Prabhakaran Soundararajan; Vadivelmurugan Irulappan; Jung Sun Kim

doi:10.7717/peerj.15696

In-silico, evolutionary, and functional analysis of CHUP1 and its related proteins in Bienertia sinuspersici-a comparative study across C₃, C₄, CAM, and SCC₄ model plants

PeerJ. 2023 Jul 11:11:e15696. doi: 10.7717/peerj.15696. eCollection 2023.

Authors

So Youn Won^#¹, Prabhakaran Soundararajan^#¹, Vadivelmurugan Irulappan¹, Jung Sun Kim¹

Affiliation

¹ Department of Agricultural Biotechnology, National Institute of Agricultural Sciences, Rural Development Administration, Jeonju-si, Jeollabuk-do, South Korea.

^# Contributed equally.

Abstract

Single-cell C₄ (SCC₄) plants with bienertioid anatomy carry out photosynthesis in a single cell. Chloroplast movement is the underlying phenomenon, where chloroplast unusual positioning 1 (CHUP1) plays a key role. This study aimed to characterize CHUP1 and CHUP1-like proteins in an SCC₄ photosynthetic plant, Bienertia sinuspersici. Also, a comparative analysis of SCC4 CHUP1 was made with C₃, C₄, and CAM model plants including an extant basal angiosperm, Amborella. The CHUP1 gene exists as a single copy from the basal angiosperms to SCC₄ plants. Our analysis identified that Chenopodium quinoa, a recently duplicated allotetraploid, has two copies of CHUP1. In addition, the numbers of CHUP1-like and its associated proteins such as CHUP1-like_a, CHUP1-like_b, HPR, TPR, and ABP varied between the species. Hidden Markov Model analysis showed that the gene size of CHUP1-like_a and CHUP1-like_b of SCC₄ species, Bienertia, and Suaeda were enlarged than other plants. Also, we identified that CHUP1-like_a and CHUP1-like_b are absent in Arabidopsis and Amborella, respectively. Motif analysis identified several conserved and variable motifs based on the orders (monocot and dicot) as well as photosynthetic pathways. For instance, CAM plants such as pineapple and cactus shared certain motifs of CHUP1-like_a irrespective of their distant phylogenetic relationship. The free ratio model showed that CHUP1 maintained purifying selection, whereas CHUP1-like_a and CHUP1-like_b have adaptive functions between SCC₄ plants and quinoa. Similarly, rice and maize branches displayed functional diversification on CHUP1-like_b. Relative gene expression data showed that during the subcellular compartmentalization process of Bienertia, CHUP1 and actin-binding proteins (ABP) genes showed a similar pattern of expression. Altogether, the results of this study provide insight into the evolutionary and functional details of CHUP1 and its associated proteins in the development of the SCC₄ system in comparison with other C₃, C₄, and CAM model plants.

Keywords: Bienertia sinuspersici; CHUP1 protein; CHUP1-like proteins; Phylogenetic analysis; Single-Cell C4 plants; Subcellular compartmentalization.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Arabidopsis Proteins* / genetics
Arabidopsis* / metabolism
Carrier Proteins / genetics
Chenopodiaceae*
Chloroplasts / genetics
Magnoliopsida* / metabolism
Microfilament Proteins / genetics
Photosynthesis
Phylogeny

Substances

Microfilament Proteins
SCC4 protein, Arabidopsis
Carrier Proteins
Arabidopsis Proteins

Grants and funding

This study was supported by “The Cooperative Research Program for Rural Development Administration (PJ010953032019), Republic of Korea. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.