The genome assembly of the European aspen Populus tremula proved difficult for a short-read based strategy due to high genomic variation. As a consequence, the fragmented sequence is impeding studies that benefit from highly contiguous data, particularly genome-wide association studies (GWAS) and comparative genomics. Here we present an updated assembly based on long-read sequences, optical mapping and genetic mapping. This assembly - henceforth referred to as Potra V2 - is assembled into 19 contiguous chromosomes which provides a powerful tool for future association studies. The genome sequence and any feature files are available from the PopGenIE resource.

/pdf/an-improved-genome-assembly-of-the-european-aspen-populus-2vewyo79az.pdf

An improved genome assembly of the European aspen Populus tremula

Phytophthora pathogens lead to numerous economically damaging plant diseases worldwide, including potato late blight caused by P. infestans and soybean root rot caused by P. sojae. Our previous work showed that Phytophthora pathogens may generate abundant phosphatidylinositol 3-phosphate (PI3P) to promote infection via direct association with RxLR effectors. Here, we designed a disease control strategy for metabolizing pathogen-derived PI3P by expressing secreted Arabidopsis thaliana phosphatidylinositol-4-phosphate 5-kinase 1 (AtPIP5K1), which can phosphorylate PI3P to PI(3,4)P2. We fused AtPIP5K1 with the soybean PR1a signal peptide (SP-PIP5K1) to enable its secretion into the plant apoplast. Transgenic soybean and potato plants expressing SP-PIP5K1 showed substantially enhanced resistance to various P. sojae and P. infestans isolates, respectively. SP-PIP5K1 significantly reduced PI3P accumulation during P. sojae and soybean interaction. Knockout or inhibition of PI3 kinases (PI3Ks) in P. sojae compromised the resistance mediated by SP-PIP5K1, indicating that SP-PIP5K1 action requires a supply of pathogen-derived PI3P. Furthermore, we revealed that SP-PIP5K1 can interfere with the action of P. sojae mediated by the RxLR effector Avr1k. This novel disease control strategy has the potential to confer durable broad-spectrum Phytophthora resistance in plants through a clear mechanism in which catabolism of PI3P interferes with RxLR effector actions. 

Engineering crop Phytophthora resistance by targeting pathogen-derived PI3P for enhanced catabolism

Phosphatidylinositol 4-phosphate 5-kinase (PIP5K) is a key enzyme producing the signaling lipid phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P2 ] in eukaryotes. Although PIP5K genes are reported to be involved in pollen tube germination and growth, the essential roles of PIP5K in these processes remain unclear. Here, we performed a comprehensive genetic analysis of the Arabidopsis thaliana PIP5K4, PIP5K5, and PIP5K6 genes and revealed that their redundant function is essential for pollen germination. Pollen with the pip5k4pip5k5pip5k6 triple mutation was sterile, while pollen germination efficiency and pollen tube growth were reduced in the pip5k6 single mutant and further reduced in the pip5k4pip5k6 and pip5k5pip5k6 double mutants. YFP-fusion proteins, PIP5K4-YFP, PIP5K5-YFP, and PIP5K6-YFP, which could rescue the sterility of the triple mutant pollen, preferentially localized to the tricolpate aperture area and the future germination site on the plasma membrane prior to germination. Triple mutant pollen grains under the germination condition, in which spatiotemporal localization of the PtdIns(4,5)P2 fluorescent marker protein 2xmCHERRY-2xPHPLC as seen in the wild type was abolished, exhibited swelling and rupture of the pollen wall, but neither the conspicuous protruding site nor site-specific deposition of cell wall materials for germination. These data indicate that PIP5K4-6 and their product PtdIns(4,5)P2 are essential for pollen germination, possibly through the establishment of the germination polarity in a pollen grain.

Redundant function of the Arabidopsis phosphatidylinositol 4-phosphate 5-kinase genes PIP5K4-6 is essential for pollen germination.

During plant fertilisation, excess male gametes compete for a limited number of female gametes. The dormant male gametophyte, encapsulated in the pollen grain, consists of two sperm cells enclosed in a vegetative cell. After reaching the stigma of a compatible flower, quick and efficient germination of the vegetative cell to a tip-growing pollen tube is crucial to ensure fertilisation success. RHO OF PLANTS (ROP) signalling and their activating ROP GUANINE NUCLEOTIDE EXCHANGE FACTORS (ROPGEFs) are essential for initiating polar growth processes in multiple cell types. However, which ROPGEFs activate pollen germination is unknown. We investigated the role of ROPGEFs in initiating pollen germination and the required cell polarity establishment. Of the five pollen-expressed ROPGEFs, we found that GEF8, GEF9, and GEF12 are required for pollen germination and male fertilisation success, as gef8;gef9;gef12 triple mutants showed almost complete loss of pollen germination in vitro and had a reduced allele transmission rate. Live cell imaging and spatiotemporal analysis of subcellular protein distribution showed that GEF8 and GEF9, but not GEF12, displayed transient polar protein accumulations at the future site of pollen germination minutes before pollen germination, demonstrating specific roles for GEF8 and GEF9 during the initiation of pollen germination. Furthermore, this novel GEF accumulation appears in a biphasic temporal manner and can shift its location. We showed that the C-terminal domain of GEF8 and GEF9 confers this protein accumulation and demonstrated that GEFs locally activate ROPs and alter Ca2+ signalling, which is required for pollen tube germination. We demonstrated that GEFs do not act redundantly during pollen germination and described for the first time a polar domain with spatiotemporal flexibility, which is crucial for the de novo establishment of a polar growth domain within a cell and, thus, for pollen function and fertilisation success.

Polarised subcellular activation of ROPs by specific ROPGEFs drives pollen germination in Arabidopsis thaliana

OUP accepted manuscript

Phosphatidylinositol 4-phosphate 5-kinase (PIP5K) is involved in regulating various cellular processes through the signaling function of its product, phosphatidylinositol (4,5)-bisphosphate. Higher plants encode a large number of PIP5Ks forming distinct clades in their molecular phylogenetic tree. Although biological functions of PIP5K genes have been analyzed intensively in Arabidopsis thaliana, it remains unclear how those functions differ across clades of paralogs. We performed comparative functional analysis of the Arabidopsis genes encoding PIP5K1, PIP5K2 and PIP5K3, of which the first two and the last belong to closely related but distinct clades, to clarify their conserved and/or differentiated functions. Genetic analysis with their single and multiple mutants revealed that PIP5K1 and PIP5K3 have non-overlapping functions, with the former in total plant growth and the latter in root hair elongation, whereas PIP5K2 redundantly functions in both phenomena. This pattern of functional redundancy is explainable in terms of the overlapping pattern of their promoter activities. In transformation rescue experiments, PIP5K3 promoter-directed PIP5K1-YFP completely rescued the short-root-hair phenotype of pip5k3. However, PIP5K3-YFP could substitute for PIP5K1-YFP only partially in rescuing the severe dwarfism of pip5k1pip5k2 when directed by the PIP5K1 promoter. Phylogenetic analysis of angiosperm PIP5Ks revealed that PIP5K3 orthologs have a faster rate of diversification in their amino-acid sequences compared with PIP5K1/2 orthologs after they arose through a eudicot-specific duplication event. These findings suggest that PIP5K3 specialized to promote root hair elongation and lost some of the protein-encoded functions retained by PIP5K1 and PIP5K2, whereas PIP5K1 differentiated from PIP5K2 only in its promoter-directed expression pattern.

/pdf/functional-differentiation-among-the-arabidopsis-3bfx0dtb.pdf

Functional Differentiation among the Arabidopsis Phosphatidylinositol 4-Phosphate 5-Kinase Genes PIP5K1, PIP5K2 and PIP5K3.

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Functional Differentiation among the Arabidopsis Phosphatidylinositol 4-Phosphate 5-Kinase Genes PIP5K1, PIP5K2 and PIP5K3.

Redundant function of the Arabidopsis phosphatidylinositol 4-phosphate 5-kinase genes PIP5K4-6 is essential for pollen germination.