bims-plasge 2020-07-05 papers

Mol Biol Evol. 2020 Jun 30. pii: msaa158. [Epub ahead of print]

Co-evolution in hybrid genomes: nuclear-encoded rubisco small subunits and their plastid-targeting translocons accompanying sequential allopolyploidy events in Triticum.

Changping Li, Xiaofei Wang, Yaxian Xiao, Xuhan Sun, Jinbin Wang, Xuan Yang, Yuchen Sun, Yan Sha, Ruili Lv, Yanan Yu, Baoxu Ding, Zhibin Zhang, Ning Li, Tianya Wang, Jonathan F Wendel, Bao Liu, Lei Gong.

The Triticum/Aegilops complex includes hybrid species resulting from HHS (homoploid hybrid speciation) and AS (allopolyploid speciation). Sequential allotetra- and allohexaploidy events presumably result in two challenges for the hybrids, which involve (i) cytonuclear stoichiometric disruptions caused by combining two diverged nuclear genomes with the maternal inheritance of the cytoplasmic organellar donor; and (ii) incompatibility of chimeric protein complexes with diverged subunits from nuclear and cytoplasmic genomes. Here, we describe co-evolution 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.

Keywords: Triticum/Aegilops complex; CECs; Cytonuclear coordination; Hybrid species; Rubisco; Translocon

DOI: https://doi.org/10.1093/molbev/msaa158

Front Plant Sci. 2020 ;11 814

PPR14 Interacts With PPR-SMR1 and CRM Protein Zm-mCSF1 to Facilitate Mitochondrial Intron Splicing in Maize.

Hong-Chun Wang, Zongliang Chen, Yan-Zhuo Yang, Feng Sun, Shuo Ding, Xiu-Lan Li, Chunhui Xu, Bao-Cai Tan.

In plants, splicing of organellar group II introns involves numerous nucleus-encoded trans-factors. But, how these trans-factors function and interact is not well understood. Here we report the function of a pentatricopeptide repeat (PPR) protein PPR14 and its physical relationship with other splicing factors in mitochondria. Null mutations of PPR14 severely arrest the embryo and endosperm development, causing an empty pericarp phenotype. PPR14 is required for the splicing of NADH dehydrogenase 2 (nad2) intron 3 and nad7 introns 1 and 2 in mitochondria. The absence of nad2 and nad7 transcripts leads to disruption of the mitochondrial complex I assembly and abolishes its NADH dehydrogenase activity. This is accompanied with increased levels of other mitochondrial complexes and elevated expression of the alternative oxidase proteins. As the function of PPR14 overlaps with PPR-SMR1 and the CRM-domain containing protein Zm-mCSF1, we tested their interactions. Protein-protein interaction analysis indicated that PPR14 interacts with PPR-SMR1 and Zm-mCSF1, suggesting that these three proteins may form a complex. As PPR proteins and CRM-domain containing proteins have many members in mitochondria and chloroplasts, we propose that organellar group II intron splicing is probably mediated by a dynamic complex that includes different PPR and CRM proteins in plants.

Keywords: interaction; intron splicing; maize; mitochondria; pentatricopeptide repeat (PPR) protein; seed development

DOI: https://doi.org/10.3389/fpls.2020.00814

Front Plant Sci. 2020 ;11 749

The Rice Pentatricopeptide Repeat Protein PPR756 Is Involved in Pollen Development by Affecting Multiple RNA Editing in Mitochondria.

Qiannan Zhang, Yanghong Xu, Jishuai Huang, Kai Zhang, Haijun Xiao, Xiaojian Qin, Linlin Zhu, Yingguo Zhu, Jun Hu.

In land plants, the pentatricopeptide repeat (PPR) proteins form a large family involved in post-transcriptional processing of RNA in mitochondria and chloroplasts, which is critical for plant development and evolutionary adaption. Although studies showed a number of PPR proteins generally influence the editing of organellar genes, few of them were characterized in detail in rice. Here, we report a PLS-E subclass PPR protein in rice, PPR756, loss of function of which led to the abolishment of RNA editing events among three mitochondrial genes including atp6, ccmC, and nad7. Their defective C-to-U transformation then resulted in improper amino acid retention which could cause abortive pollen development. Furthermore, PPR756 could bind to the three target genes directly and interact with three OsMORFs (multiple organellar RNA editing factors): OsMORF1, OsMORF8-1, and OsMORF8-2. The knock-out plants of PPR756 exhibited retarded growth and greener leaves during the early vegetative stages, along with sterile pollen and lower seed setting at the reproductive stage. These results established a role for PPR756 in rice development, participating in RNA editing of three various transcripts and cooperating with OsMORFs via an editosome manner in rice.

Keywords: OsMORFs; RNA editing; chloroplasts; mitochondria; pentatricopeptide repeat (PPR) proteins; sterility

DOI: https://doi.org/10.3389/fpls.2020.00749

Theor Appl Genet. 2020 Jul 01.

Identification and editing of a hybrid lethality gene expands the range of interspecific hybridization potential in Nicotiana.

Justin Ma, Wesley G Hancock, Jessica M Nifong, Sheri P Kernodle, Ramsey S Lewis.

KEY MESSAGE: Identification and inactivation of hybrid lethality genes can be used to expand the available gene pool for improvement of a cultivated crop species. Hybrid lethality is one genetic mechanism that contributes to reproductive isolation in plants and serves as a barrier to use of diverse germplasm for improvement of cultivated species. A classic example is the seedling lethality exhibited by progeny from the Nicotiana tabacum × N. africana interspecific cross. In order to increase the body of knowledge on mechanisms of hybrid lethality in plants, and to potentially develop tools to circumvent them, we utilized a transposon tagging strategy to identify a candidate gene involved in the control of this reaction. N. tabacum gene Nt6549g30 was identified to code for a class of coiled-coil nucleotide-binding site-leucine-rich repeat (CC-NBS-LRR) proteins, the largest class of plant defense proteins. Gene editing, along with other experiments, was used to verify that Nt6549g30 is the gene at the N. tabacum Hybrid Lethality 1 (NtHL1) locus controlling the hybrid lethality reaction in crosses with N. africana. Gene editing of Nt6549g30 was also used to reverse interspecific seedling lethality in crosses between N. tabacum and eight of nine additional tested species from section Suaveolentes. Results further implicate the role of disease resistance-like genes in the evolution of plant species and demonstrate the possibility of expanding the gene pool for a crop species through gene editing.

DOI: https://doi.org/10.1007/s00122-020-03641-w