Dataset Information

Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum.

ABSTRACT: The Triticum/Aegilops complex includes hybrid species resulting from homoploid hybrid speciation and allopolyploid speciation. Sequential allotetra- and allohexaploidy events presumably result in two challenges for the hybrids, which involve 1) cytonuclear stoichiometric disruptions caused by combining two diverged nuclear genomes with the maternal inheritance of the cytoplasmic organellar donor; and 2) incompatibility of chimeric protein complexes with diverged subunits from nuclear and cytoplasmic genomes. Here, we describe coevolution of nuclear rbcS genes encoding the small subunits of Rubisco (ribulose 1,5-bisphosphate carboxylase/oxygenase) and nuclear genes encoding plastid translocons, which mediate recognition and translocation of nuclear-encoded proteins into plastids, in allopolyploid wheat species. We demonstrate that intergenomic paternal-to-maternal gene conversion specifically occurred in the genic region of the homoeologous rbcS3 gene from the D-genome progenitor of wheat (abbreviated as rbcS3D) such that it encodes a maternal-like or B-subgenome-like SSU3D transit peptide in allohexaploid wheat but not in allotetraploid wheat. Divergent and limited interaction between SSU3D and the D-subgenomic TOC90D translocon subunit is implicated to underpin SSU3D targeting into the chloroplast of hexaploid wheat. This implicates early selection favoring individuals harboring optimal maternal-like organellar SSU3D targeting in hexaploid wheat. These data represent a novel dimension of cytonuclear evolution mediated by organellar targeting and transportation of nuclear proteins.

SUBMITTER: Li C

PROVIDER: S-EPMC7743682 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Publications

Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum.

Li Changping C Wang Xiaofei X Xiao Yaxian Y Sun Xuhan X Wang Jinbin J Yang Xuan X Sun Yuchen Y Sha Yan Y Lv Ruili R Yu Yanan Y Ding Baoxu B Zhang Zhibin Z Li Ning N Wang Tianya T Wendel Jonathan F JF Liu Bao B Gong Lei L

Molecular biology and evolution 20201201 12

The Triticum/Aegilops complex includes hybrid species resulting from homoploid hybrid speciation and allopolyploid speciation. Sequential allotetra- and allohexaploidy events presumably result in two challenges for the hybrids, which involve 1) cytonuclear stoichiometric disruptions caused by combining two diverged nuclear genomes with the maternal inheritance of the cytoplasmic organellar donor; and 2) incompatibility of chimeric protein complexes with diverged subunits from nuclear and cytopla ...[more]

PMID: 32602899

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Project description:Ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (RuBisCO) is the carbon-fixing enzyme present in most photosynthetic organisms, converting CO2 into organic matter. Globally, photosynthetic efficiency in terrestrial plants has become increasingly challenged in recent decades due to a rapid increase in atmospheric CO2 and associated changes toward warmer and dryer environments. Well adapted for these new climatic conditions, the C4 photosynthetic pathway utilizes carbon concentrating mechanisms to increase CO2 concentrations surrounding RuBisCO, suppressing photorespiration from the oxygenase catalyzed reaction with O2. The energy efficiency of C3 photosynthesis, from which the C4 pathway evolved, is thought to rely critically on an uninterrupted supply of chloroplast CO2. Part of the homeostatic mechanism that maintains this constancy of supply involves the CO2 produced as a byproduct of photorespiration in a negative feedback loop. Analyzing the database of RuBisCO kinetic parameters, we suggest that in genera (Flaveria and Panicum) for which both C3 and C4 examples are available, the C4 pathway evolved only from C3 ancestors possessing much lower than the average carboxylase specificity relative to that of the oxygenase reaction (S C/O=S C/S O), and hence, the higher CO2 levels required for development of the photorespiratory CO2 pump (C2 photosynthesis) essential in the initial stages of C4 evolution, while in the later stage (final optimization phase in the Flaveria model) increased CO2 turnover may have occurred, which would have been supported by the higher CO2 levels. Otherwise, C4 RuBisCO kinetic traits remain little changed from the ancestral C3 species. At the opposite end of the spectrum, C3 plants (from Limonium) with higher than average S C/O, which may be associated with the ability of increased CO2, relative to O2, affinity to offset reduced photorespiration and chloroplast CO2 levels, can tolerate high stress environments. It is suggested that, instead of inherently constrained by its kinetic mechanism, RuBisCO possesses the extensive kinetic plasticity necessary for adaptation to changes in photorespiration that occur in the homeostatic regulation of CO2 supply under a broad range of abiotic environmental conditions.

Dataset Information

Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum.

Publications

Coevolution in Hybrid Genomes: Nuclear-Encoded Rubisco Small Subunits and Their Plastid-Targeting Translocons Accompanying Sequential Allopolyploidy Events in Triticum.

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