Comparative transcriptomics reveals the role of altered energy metabolism in the establishment of single-cell C4 photosynthesis in Bienertia sinuspersici

Abstract

Single-cell C4 photosynthesis (SCC4) in terrestrial plants without Kranz anatomy involves three steps: initial CO2 fixation in the cytosol, CO2 release in mitochondria, and a second CO2 fixation in central chloroplasts. Here, we investigated how the large number of mechanisms underlying these processes, which occur in three different compartments, are orchestrated in a coordinated manner to establish the C4 pathway in Bienertia sinuspersici, a SCC4 plant. Leaves were subjected to transcriptome analysis at three different developmental stages. Functional enrichment analysis revealed that SCC4 cycle genes are coexpressed with genes regulating cyclic electron flow and amino/organic acid metabolism, two key processes required for the production of energy molecules in C3 plants. Comparative gene expression profiling of B. sinuspersici and three other species (Suaeda aralocaspica, Amaranthus hypochondriacus, and Arabidopsis thaliana) showed that the direction of metabolic flux was determined via an alteration in energy supply in peripheral chloroplasts and mitochondria via regulation of gene expression in the direction of the C4 cycle. Based on these results, we propose that the redox homeostasis of energy molecules via energy metabolism regulation is key to the establishment of the SCC4 pathway in B. sinuspersici.

Elucidating the callus-to-shoot-forming mechanism in Capsicum annuum ‘Dempsey’ through comparative transcriptome analyses

“…The low-expression genes were filtered out, and the Trimmed Mean of M-values (TMM)-normalized counts were obtained based on Counts Per Million (CPM) value of more than 1 in at least one sample. Second, non-DEGs were filtered using the NOISeq package with a ranking score (RS) of 20.1, based on an Euclidean distance of the fold change (FC) of more than 2 and an absolute expression difference (D) greater than 20 between the TMM-normalized counts [ 38 , 39 ]. After filtering non-DEGs, a heatmap was generated, and the subsequent DEGs were clustered into six K-means clusters using Morpheus software ( https://software.broadinstitute.org/morpheus ).…”

“…We focused on callus and shoot-specific gene regulation by identifying DEGs between leaf/seedling and callus and leaf/seedling and shoot RNA-seq samples, thereby discerning upregulated and downregulated genes in the callus and shoot tissues compared to basal control. In the comparative datasets, we identified all DEGs using an FDR < 0.05 in ‘Dempsey’ and A. thaliana and a probability value (q) of > 0.8 in Petunia spp., using a previously described method [ 39 ]. The Arabidopsis Hormone Database 2.0 (AHD2.0) and the R package org.At.tair.db were utilized for analyzing the relationships between phytohormones and DEGs in the five species [ 43 , 48 ].…”

Genome-wide identification of a novel Na+ transporter from Bienertia sinuspersici and overexpression of BsHKT1;2 improved salt tolerance in Brassica rapa

“…To identify HKT gene families in the B. sinuspersici genome, the hidden Markov model (HMM) file of the cation transport protein TrkH (PF02386; https://www.ebi.ac.uk/interpro/entry/pfam/PF02386/ ) was employed and searched against whole-genome peptides and the transcriptome of B. sinuspersici (genome annotation is underway; BS790c1g1i2 in the transcriptome) ( Han et al., 2023 ). Repeated and truncated proteins were removed.…”

“…sinuspersici is a single-cell C 4 plant with non-Kranz photosynthetic anatomy (Akhani et al, 2005;Offermann et al, 2015;Koteyeva et al, 2016;Soundararajan et al, 2019). B. sinuspersici possesses dimorphic chloroplasts in a single cell, namely central and peripheral chloroplasts, unlike other C 4 plants (Offermann et al, 2015;Koteyeva et al, 2016;Mai et al, 2019;Han et al, 2023;Won et al, 2023). B. sinuspersici is a salt-tolerant halophyte belonging to the family Amaranthaceae sensu lato (Kapralov et al, 2012;Han et al, 2023) and possesses salt glands in its leaves.…”

Blazing a trail towards higher photosynthetic efficiency : A multi-dimensional study of Hirschfeldia incana

“…Technological development, however, has progressed for other disciplines as well, offering promising tools for further expanding the scope of multidisciplinary photosynthesis research. Advancements in sequencing technology and data analysis have largely benefited the field of transcriptomics, making detailed studies of the transcriptional signature of photosynthetic responses possible in many plant species (Miller et al, 2017;Xiong et al, 2019;Loudya et al, 2021;An et al, 2022;Han et al, 2023), as well as the study of photosynthetic responses to novel agronomic practices (Song et al, 2020;Zhu et al, 2023;Chai et al, 2023). In the context of genomics and transcriptomics, the development of pangenomics approaches aimed at surpassing the compression of large sets of genomic and transcriptomic sequences into single consensus assemblies has opened up new avenues for the identification of novel genetic variants for crop improvement (Tao et al, 2019;Zanini et al, 2022;Chapman et al, 2022) and will allow for the exploration of photosynthesis-related genes and transcriptional patterns from a novel perspective.…”