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The Draft Genome of Tropical Fruit Durian (Durio Zibethinus)

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ARTICLES OPEN The draft genome of tropical fruit durian (Durio zibethinus) Bin Tean Teh1–6,18 , Kevin Lim2,7,18 , Chern Han Yong2,7,18, Cedric Chuan Young Ng3,18, Sushma Ramesh Rao8–11, Vikneswari Rajasegaran3, Weng Khong Lim2,4,7 , Choon Kiat Ong12 , Ki Chan13, Vincent Kin Yuen Cheng14, Poh Sheng Soh15, Sanjay Swarup8–11,16, Steven G Rozen2,4,7 , Niranjan Nagarajan17 & Patrick Tan1,2,4,5,17 Durian (Durio zibethinus) is a Southeast Asian tropical plant known for its hefty, spine-covered fruit and sulfury and onion- like odor. Here we present a draft genome assembly of D. zibethinus, representing the third plant genus in the Malvales order and first in the Helicteroideae subfamily to be sequenced. Single-molecule sequencing and chromosome contact maps enabled assembly of the highly heterozygous durian genome at chromosome-scale resolution. Transcriptomic analysis showed upregulation of sulfur-, ethylene-, and lipid-related pathways in durian fruits. We observed paleopolyploidization events shared by durian and cotton and durian-specific gene expansions in MGL (methionine g-lyase), associated with production of volatile sulfur compounds (VSCs). MGL and the ethylene-related gene ACS (aminocyclopropane-1-carboxylic acid synthase) were upregulated in fruits concomitantly with their downstream metabolites (VSCs and ethylene), suggesting a potential association between ethylene biosynthesis and methionine regeneration via the Yang cycle. The durian genome provides a resource for tropical fruit biology and agronomy. Durian (D. zibethinus) is an edible tropical fruit endemic to Southeast cultivars reflect local idiosyncrasies in consumer tastes: pungent and Asia. In the region, durian is known as the ‘king of fruits’ for its formi- bitter varieties are prized in Malaysia and Singapore (for example, dable spiny husk, overpowering flavor, and unique odor, described as Musang King), whereas sweeter cultivars with a mild odor are popu- an onion-like, sulfury aroma with notes of sweet fruitiness and savory lar in Thailand (for example, Monthong). The distinctive odors of soup seasoning1. Durian can elicit opposing opinions, from devotion different durian cultivars have also been biochemically studied and to revulsion; the famed naturalist Alfred Russel Wallace once remarked characterized as a complex suite of odor-active compounds including on durian: “the more you eat of it, the less you feel inclined to stop” sulfur volatiles, esters, alcohols, and acids4–6. (ref. 2). In contrast, durian is banned from public transportation and Despite the importance of durian as a tropical fruit crop, durian- many hotels because of its characteristic and pungent smell, described related genetic research is almost nonexistent. Important resources by some detractors as “turpentine and onions, garnished with a gym such as genetic maps are not publicly available for durian, and sock” (ref. 3). no plant species in the Helicteroideae subfamily have had their Among the 30 known species in the Durio genus, D. zibethinus is the genomes sequenced and assembled. Relatives whose genomes are most prized as a major Southeast Asian food crop. The three leading available include only the more distantly related cash crops within durian-producing countries are Thailand, Malaysia, and Indonesia, the larger Malvaceae family: Theobroma cacao (cacao; used in © 2017 Nature America, Inc., part of Springer Nature. All rights reserved. All rights part Nature. of Springer Inc., America, Nature © 2017 with more than 250,000 ha cultivated in 2008 (ref. 4). Durian is also of chocolate) and members of the Gossypium genus (cotton). Besides major economic value, as it has recently gained market penetrance in D. zibethinus, several other Durio species can produce edible fruits China: in 2016 alone, durian imports into China accounted for about (for example, Durio graveolens and Durio testudinarum), occupy- $600 million, as compared to $200 million for oranges, one of China’s ing specific ecological niches where they have relationships with other main fruit imports (UN Trade Statistics; see URLs). More than specific pollinators, primarily fruit bats and birds1,7. However, 200 different cultivars of durian exist, encompassing a range of fruit many of the other Durio species are currently listed as vulnerable textures, flavors, and aromas. Distinct regional demands for different or endangered. 1Thorn Biosystems Pte Ltd, Singapore. 2Program in Cancer and Stem Cell Biology, Duke-NUS Medical School, Singapore. 3Laboratory of Cancer Epigenome, Division of Medical Science, National Cancer Centre singapore, Singapore. 4SingHealth/Duke-NUS Institute of Precision Medicine, National Heart Centre, Singapore. 5Cancer Science Institute of Singapore, National University of Singapore, Singapore. 6Institute of Molecular and Cellular Biology, Singapore. 7Centre for Computational Biology, Duke-NUS Medical School, Singapore. 8Department of Biological Sciences, National University of Singapore, Singapore. 9Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, Singapore. 10Metabolites Biology Laboratory, National University of Singapore, Singapore. 11NUS Synthetic Biology for Clinical and Technological Innovation, Life Sciences Institute, National University of Singapore, Singapore. 12Lymphoma Genomic Translational Research Laboratory, National Cancer Centre, Singapore. 13Global Databank, Singapore. 14Verdant Foundation, Hong Kong. 15Samsoney Group, Johor Bahru, Malaysia. 16NUS Environmental Research Institute, National University of Singapore, Singapore. 17Genome Institute of Singapore, Singapore. 18These authors contributed equally to this work. Correspondence should be addressed to B.T.T. ([email protected]) or P.T. ([email protected]). Received 21 June; accepted 18 September; published online 9 October 2017; doi:10.1038/ng.3972 NATURE GENETICS VOLUME 49 | NUMBER 11 | NOVEMBER 2017 1633 ARTICLES dz1 40 35 30 dz21 25 20 15 0 5 tc10 10 20 10 15 25 30 dz26 35 0 20 5 5 Here we report a draft whole-genome assembly of the D. zibethinus 10 0 15 15 a 10 0 tc9 5 10 dz2 5 15 0 0 20 5 15 10 10 1 tc8 15 20 Musang King cultivar, employing a combination of sequencing tech- 5 25 0 30 25 35 dz8 20 0 15 5 tc710 2 10 15 5 20 nologies. We used the durian genome to assess phylogenetic relation- 40 0 25 dz9 o 35 0 30 5 a 25 10 c 20 3 15 tc615 20 dz19 a 10 25 ships with other Malvaceae members and to compare transcriptome 0 c 5 5 0 10 . 30 4 15 T 25 20 20 0 dz6 data between different plant organs (fruit aril, leaf, stem, and root) 5 tc515 D 10 10 15 5 20 . 0 25 dz10 z and between fruit arils from different cultivars. Genomic and tran- 30 0 i 25 5 b 20 10 15 15 e tc410 20 t dz11 scriptomic analyses provided insights into the evolution and regula- 5 h 0 0 5 i 40 10 n 35 15 30 20 u tion of fruit-related processes in durian, including ripening, flavonoid 25 s 20 0 tc3 15 5 10 10 5 15 0 20 production, and sulfur metabolism. The durian genome provides a dz4 25 35 30 30 0 tc2 25 5 valuable resource for biological research and agronomy of this tropi- 20 10 15 15 10 20 5 0 0 dz15 5 cal fruit. 25 10 20 tc1 15 15 10 20 5 0 dz13 0 5 10 15 dz29 20 10 25 5 0 dz7 0 5 RESULTS 10 dz2715 15 105 0 0 5 dz22 dz2415 10 10 15 5 20 Genome assembly 0 0 5 15 10 dz2510 5 15 dz16 0 0 5 10 20 15 15 20 dz28 We extracted DNA from a D. zibethinus Musang King durian fruit dz14 10 5 0 0 5 10 15 10 5 0 0 dz30 5 10 dz17 15 25 20 20 5 0 15 10 5 15 0 10 25 20 30 5 0 dz20 15 0 stalk, generating 18.3 million PacBio single-molecule long reads dz5 10 5 20 dz23 15 10 dz12 (average read length of 6.2 kb) corresponding to ~153× coverage dz18 dz3 CMC-EnSpm 4.0% of the ~738-Mb durian genome whose size was estimated by k-mer b hAT-Ac 1.0% Other DNA 0.9% distribution analysis (Supplementary Fig. 1 and Supplementary hAT-Tag1 0.4% 6% PIF-Harbinger 0.3% Table 1). We performed a PacBio-only assembly using an overlap- Copia Zisupton 0.3% 8 0.7% Caulimovirus MULE-MuDR 0.2% layout-consensus method implemented in FALCON ; as the durian Maverick 0.1% genome is highly heterozygous, possibly owing to frequent outcrossing hAT-Tip100 0.1% Gypsy L1 1.0% 48% LTR Repeats RTE-BovB 0.3% during cultivation, we additionally phased the contigs using diploid- 30% Unknown aware FALCON-Unzip9. The subsequent haplotig-merged assem- L2 0.02% DNA rRNA 5.0% LINE bly was polished using Arrow over three iterations. For details on RC validation of the genome assembly, see the Supplementary Note. Helitron 5.0% The durian assembly was further refined in two stages using chro- Satellite 1% mosome contact maps. CHiCAGO (in vitro chromatin reconstitu- Simple repeat 0.2% tRNA 0.005% tion of high-molecular-weight DNA) and Hi-C (in vivo fixation of SINE 0.0002% chromosomes) libraries10,11 (~280 million read pairs each) were used to improve scaffold N50 to 22.7 Mb, with the longest scaffold e s c Nucleic acid n being 36.3 Mb (Fig. 1a; GC content of 32.5%). The final reference metabolic e f process 12% esnopser eD assembly comprised chromosome-scale pseudomolecules, with 30 %0 7% Small pseudomolecules greater than 10 Mb in length and covering 95% of molecule 1 metabolic process the 712-Mb assembly (the pseudomolecules are hereafter referred to Protein metabolic 5% Fruit as chromosomes, numbered according to size; Table 1). These figures process 8% development Gene 6% Organelle 3% Carbohydrate correspond closely to previous estimates of the haploid chromosome Ontology organization metabolic process 12 5% Flower number of durian (1n = 28, 2n = 56) .
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    WHAT TO EAT ON THE AUTOIMMUNE PROTOCOL All the foods listed here are great to include in your It’s time to create an epidemic of - health. And it starts with learning ents that will help regulate your immune system and how to eat more nutrient-dense food. your hormones and provide the building blocks that your body needs to heal. You don’t need to eat all of these foods (it’s okay if snails, frog legs, and crickets aren’t your thing, and it’s okay if you just can’t get kangaroo meat or mizuna), but the idea is both to give Poultry innovative ways to increase variety and nutrient density • chicken • grouse • pigeon by exploring new foods. • dove • guinea hen • quail • duck • ostrich • turkey • emu • partridge (essentially, Red Meat • goose • pheasant any bird) • antelope • deer • mutton • bear • elk • pork • beaver • goat • rabbit • beef • hare • sea lion • • horse • seal • boar • kangaroo • whale • camel • lamb (essentially, • caribou • moose any mammal) Amphibians and Reptiles • crocodile • frog • snake • turtle 1 22 Fish* Shellfish • anchovy • gar • • abalone • limpet • scallop • Arctic char • haddock • salmon • clam • lobster • shrimp • Atlantic • hake • sardine • cockle • mussel • snail croaker • halibut • shad • conch • octopus • squid • barcheek • herring • shark • crab • oyster • whelk goby • John Dory • sheepshead • • periwinkle • bass • king • silverside • • prawn • bonito mackerel • smelt • bream • lamprey • snakehead • brill • ling • snapper • brisling • loach • sole • carp • mackerel • • • mahi mahi • tarpon • cod • marlin • tilapia • common dab • • • conger • minnow • trout • crappie • • tub gurnard • croaker • mullet • tuna • drum • pandora • turbot Other Seafood • eel • perch • walleye • anemone • sea squirt • fera • plaice • whiting • caviar/roe • sea urchin • • pollock • • *See page 387 for Selenium Health Benet Values.
  • Complete Chloroplast Genomes Shed Light on Phylogenetic

    Complete Chloroplast Genomes Shed Light on Phylogenetic

    www.nature.com/scientificreports OPEN Complete chloroplast genomes shed light on phylogenetic relationships, divergence time, and biogeography of Allioideae (Amaryllidaceae) Ju Namgung1,4, Hoang Dang Khoa Do1,2,4, Changkyun Kim1, Hyeok Jae Choi3 & Joo‑Hwan Kim1* Allioideae includes economically important bulb crops such as garlic, onion, leeks, and some ornamental plants in Amaryllidaceae. Here, we reported the complete chloroplast genome (cpDNA) sequences of 17 species of Allioideae, fve of Amaryllidoideae, and one of Agapanthoideae. These cpDNA sequences represent 80 protein‑coding, 30 tRNA, and four rRNA genes, and range from 151,808 to 159,998 bp in length. Loss and pseudogenization of multiple genes (i.e., rps2, infA, and rpl22) appear to have occurred multiple times during the evolution of Alloideae. Additionally, eight mutation hotspots, including rps15-ycf1, rps16-trnQ-UUG, petG-trnW-CCA , psbA upstream, rpl32- trnL-UAG , ycf1, rpl22, matK, and ndhF, were identifed in the studied Allium species. Additionally, we present the frst phylogenomic analysis among the four tribes of Allioideae based on 74 cpDNA coding regions of 21 species of Allioideae, fve species of Amaryllidoideae, one species of Agapanthoideae, and fve species representing selected members of Asparagales. Our molecular phylogenomic results strongly support the monophyly of Allioideae, which is sister to Amaryllioideae. Within Allioideae, Tulbaghieae was sister to Gilliesieae‑Leucocoryneae whereas Allieae was sister to the clade of Tulbaghieae‑ Gilliesieae‑Leucocoryneae. Molecular dating analyses revealed the crown age of Allioideae in the Eocene (40.1 mya) followed by diferentiation of Allieae in the early Miocene (21.3 mya). The split of Gilliesieae from Leucocoryneae was estimated at 16.5 mya.