Allele-dependent expression and functionality of lipid enzyme phospholipid:diacylglycerol acyltransferase affect diatom carbon storage and growth
2023
Pan, Yufang | Zhang, Wanting | Wang, Xiaofei | Jouhet, Juliette | Maréchal, Eric | Liu, Jin | Xia, Xiao-Qin | Hu, Hanhua | Institute of Hydrobiology - Chinese Academy of Sciences ; Marine and Estuarine Fisheries (Ministry of Agriculture) | Laboratory for Algae Biotechnology and Innovation, Peking University | LIPID ; Physiologie cellulaire et végétale (LPCV) ; Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG) ; Direction de Recherche Fondamentale (CEA) (DRF (CEA)) ; Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) ; Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG) ; Direction de Recherche Fondamentale (CEA) (DRF (CEA)) ; Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) ; Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA) | National Natural Science Foundation of China (41976119, 42376131, and 31800302) | International Partnership Program of Chinese Academy of Sciences (Grant No. 075GJHZ2022014MI) | ANR-10-LABX-0049,GRAL,Grenoble Alliance for Integrated Structural Cell Biology(2010) | ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017) | ANR-15-IDEX-0002,UGA,IDEX UGA(2015) | ANR-20-CE02-0020,ALPALGA,Microalgues des Alpes(2020) | ANR-21-CE02-0021,Dim,Croissance des micro-algues à très faibles lumières sous la banquise arctique à la sortie de la nuit polaire, et rôle dans l'inoculation du bloom printanier(2021)
Abstract In the acyl-CoA-independent pathway of triacylglycerol (TAG) synthesis unique to plants, fungi, and algae, TAG formation is catalyzed by the enzyme phospholipid:diacylglycerol acyltransferase (PDAT). The unique PDAT gene of the model diatom Phaeodactylum tricornutum strain CCMP2561 boasts 47 single nucleotide variants within protein coding regions of the alleles. To deepen our understanding of TAG synthesis, we observed the allele-specific expression of PDAT by the analysis of 87 published RNA-sequencing (RNA-seq) data and experimental validation. The transcription of one of the two PDAT alleles, Allele 2, could be specifically induced by decreasing nitrogen concentrations. Overexpression of Allele 2 in P. tricornutum substantially enhanced the accumulation of TAG by 44% to 74% under nutrient stress; however, overexpression of Allele 1 resulted in little increase of TAG accumulation. Interestingly, a more serious growth inhibition was observed in the PDAT Allele 1 overexpression strains compared with Allele 2 counterparts. Heterologous expression in yeast (Saccharomyces cerevisiae) showed that enzymes encoded by PDAT Allele 2 but not Allele 1 had TAG biosynthetic activity, and 7 N-terminal and 3 C-terminal amino acid variants between the 2 allele-encoded proteins substantially affected enzymatic activity. P. tricornutum PDAT, localized in the innermost chloroplast membrane, used monogalactosyldiacylglycerol and phosphatidylcholine as acyl donors as demonstrated by the increase of the 2 lipids in PDAT knockout lines, which indicated a common origin in evolution with green algal PDATs. Our study reveals unequal roles among allele-encoded PDATs in mediating carbon storage and growth in response to nitrogen stress and suggests an unsuspected strategy toward lipid and biomass improvement for biotechnological purposes.
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