A termite symbiotic mushroom maximizing sexual activity at growing tips of vegetative hyphae

Huei Mei Hsieh, Mei Chu Chung, Pao Yang Chen, Fei Man Hsu, Wen Wei Liao, Ai Ning Sung, Chun Ru Lin, Chung Ju Rachel Wang, Yu Hsin Kao, Mei Jane Fang, Chi-Yung Lai, Chieh Chen Huang, Jyh Ching Chou, Wen Neng Chou, Bill Chia Han Chang, Yu Ming Ju

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Background: Termitomyces mushrooms are mutualistically associated with fungus-growing termites, which are widely considered to cultivate a monogenotypic Termitomyces symbiont within a colony. Termitomyces cultures isolated directly from termite colonies are heterokaryotic, likely through mating between compatible homokaryons. Results: After pairing homokaryons carrying different haplotypes at marker gene loci MIP and RCB from a Termitomyces fruiting body associated with Odontotermes formosanus, we observed nuclear fusion and division, which greatly resembled meiosis, during each hyphal cell division and conidial formation in the resulting heterokaryons. Surprisingly, nuclei in homokaryons also behaved similarly. To confirm if meiotic-like recombination occurred within mycelia, we constructed whole-genome sequencing libraries from mycelia of two homokaryons and a heterokaryon resulting from mating of the two homokaryons. Obtained reads were aligned to the reference genome of Termitomyces sp. J132 for haplotype reconstruction. After removal of the recombinant haplotypes shared between the heterokaryon and either homokaryons, we inferred that 5.04% of the haplotypes from the heterokaryon were the recombinants resulting from homologous recombination distributed genome-wide. With RNA transcripts of four meiosis-specific genes, including SPO11, DMC1, MSH4, and MLH1, detected from a mycelial sample by real-time quantitative PCR, the nuclear behavior in mycelia was reconfirmed meiotic-like. Conclusion: Unlike other basidiomycetes where sex is largely restricted to basidia, Termitomyces maximizes sexuality at somatic stage, resulting in an ever-changing genotype composed of a myriad of coexisting heterogeneous nuclei in a heterokaryon. Somatic meiotic-like recombination may endow Termitomyces with agility to cope with termite consumption by maximized genetic variability.

Original languageEnglish
Article number39
JournalBotanical Studies
Volume58
Issue number1
DOIs
Publication statusPublished - 2017 Dec 1

Fingerprint

Termitomyces
Isoptera
heterokaryon
mushrooms
hyphae
haplotypes
mycelium
meiosis
genome
Odontotermes
basidia
DNA libraries
homologous recombination
messenger RNA
fruiting bodies
Basidiomycota
symbionts
cell division
quantitative polymerase chain reaction
genetic variation

All Science Journal Classification (ASJC) codes

  • Plant Science

Cite this

Hsieh, H. M., Chung, M. C., Chen, P. Y., Hsu, F. M., Liao, W. W., Sung, A. N., ... Ju, Y. M. (2017). A termite symbiotic mushroom maximizing sexual activity at growing tips of vegetative hyphae. Botanical Studies, 58(1), [39]. https://doi.org/10.1186/s40529-017-0191-9
Hsieh, Huei Mei ; Chung, Mei Chu ; Chen, Pao Yang ; Hsu, Fei Man ; Liao, Wen Wei ; Sung, Ai Ning ; Lin, Chun Ru ; Wang, Chung Ju Rachel ; Kao, Yu Hsin ; Fang, Mei Jane ; Lai, Chi-Yung ; Huang, Chieh Chen ; Chou, Jyh Ching ; Chou, Wen Neng ; Chang, Bill Chia Han ; Ju, Yu Ming. / A termite symbiotic mushroom maximizing sexual activity at growing tips of vegetative hyphae. In: Botanical Studies. 2017 ; Vol. 58, No. 1.
@article{730df9a865d54aa8adc92f147d917861,
title = "A termite symbiotic mushroom maximizing sexual activity at growing tips of vegetative hyphae",
abstract = "Background: Termitomyces mushrooms are mutualistically associated with fungus-growing termites, which are widely considered to cultivate a monogenotypic Termitomyces symbiont within a colony. Termitomyces cultures isolated directly from termite colonies are heterokaryotic, likely through mating between compatible homokaryons. Results: After pairing homokaryons carrying different haplotypes at marker gene loci MIP and RCB from a Termitomyces fruiting body associated with Odontotermes formosanus, we observed nuclear fusion and division, which greatly resembled meiosis, during each hyphal cell division and conidial formation in the resulting heterokaryons. Surprisingly, nuclei in homokaryons also behaved similarly. To confirm if meiotic-like recombination occurred within mycelia, we constructed whole-genome sequencing libraries from mycelia of two homokaryons and a heterokaryon resulting from mating of the two homokaryons. Obtained reads were aligned to the reference genome of Termitomyces sp. J132 for haplotype reconstruction. After removal of the recombinant haplotypes shared between the heterokaryon and either homokaryons, we inferred that 5.04{\%} of the haplotypes from the heterokaryon were the recombinants resulting from homologous recombination distributed genome-wide. With RNA transcripts of four meiosis-specific genes, including SPO11, DMC1, MSH4, and MLH1, detected from a mycelial sample by real-time quantitative PCR, the nuclear behavior in mycelia was reconfirmed meiotic-like. Conclusion: Unlike other basidiomycetes where sex is largely restricted to basidia, Termitomyces maximizes sexuality at somatic stage, resulting in an ever-changing genotype composed of a myriad of coexisting heterogeneous nuclei in a heterokaryon. Somatic meiotic-like recombination may endow Termitomyces with agility to cope with termite consumption by maximized genetic variability.",
author = "Hsieh, {Huei Mei} and Chung, {Mei Chu} and Chen, {Pao Yang} and Hsu, {Fei Man} and Liao, {Wen Wei} and Sung, {Ai Ning} and Lin, {Chun Ru} and Wang, {Chung Ju Rachel} and Kao, {Yu Hsin} and Fang, {Mei Jane} and Chi-Yung Lai and Huang, {Chieh Chen} and Chou, {Jyh Ching} and Chou, {Wen Neng} and Chang, {Bill Chia Han} and Ju, {Yu Ming}",
year = "2017",
month = "12",
day = "1",
doi = "10.1186/s40529-017-0191-9",
language = "English",
volume = "58",
journal = "Botanical Studies",
issn = "1817-406X",
publisher = "Academia Sinica",
number = "1",

}

Hsieh, HM, Chung, MC, Chen, PY, Hsu, FM, Liao, WW, Sung, AN, Lin, CR, Wang, CJR, Kao, YH, Fang, MJ, Lai, C-Y, Huang, CC, Chou, JC, Chou, WN, Chang, BCH & Ju, YM 2017, 'A termite symbiotic mushroom maximizing sexual activity at growing tips of vegetative hyphae', Botanical Studies, vol. 58, no. 1, 39. https://doi.org/10.1186/s40529-017-0191-9

A termite symbiotic mushroom maximizing sexual activity at growing tips of vegetative hyphae. / Hsieh, Huei Mei; Chung, Mei Chu; Chen, Pao Yang; Hsu, Fei Man; Liao, Wen Wei; Sung, Ai Ning; Lin, Chun Ru; Wang, Chung Ju Rachel; Kao, Yu Hsin; Fang, Mei Jane; Lai, Chi-Yung; Huang, Chieh Chen; Chou, Jyh Ching; Chou, Wen Neng; Chang, Bill Chia Han; Ju, Yu Ming.

In: Botanical Studies, Vol. 58, No. 1, 39, 01.12.2017.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A termite symbiotic mushroom maximizing sexual activity at growing tips of vegetative hyphae

AU - Hsieh, Huei Mei

AU - Chung, Mei Chu

AU - Chen, Pao Yang

AU - Hsu, Fei Man

AU - Liao, Wen Wei

AU - Sung, Ai Ning

AU - Lin, Chun Ru

AU - Wang, Chung Ju Rachel

AU - Kao, Yu Hsin

AU - Fang, Mei Jane

AU - Lai, Chi-Yung

AU - Huang, Chieh Chen

AU - Chou, Jyh Ching

AU - Chou, Wen Neng

AU - Chang, Bill Chia Han

AU - Ju, Yu Ming

PY - 2017/12/1

Y1 - 2017/12/1

N2 - Background: Termitomyces mushrooms are mutualistically associated with fungus-growing termites, which are widely considered to cultivate a monogenotypic Termitomyces symbiont within a colony. Termitomyces cultures isolated directly from termite colonies are heterokaryotic, likely through mating between compatible homokaryons. Results: After pairing homokaryons carrying different haplotypes at marker gene loci MIP and RCB from a Termitomyces fruiting body associated with Odontotermes formosanus, we observed nuclear fusion and division, which greatly resembled meiosis, during each hyphal cell division and conidial formation in the resulting heterokaryons. Surprisingly, nuclei in homokaryons also behaved similarly. To confirm if meiotic-like recombination occurred within mycelia, we constructed whole-genome sequencing libraries from mycelia of two homokaryons and a heterokaryon resulting from mating of the two homokaryons. Obtained reads were aligned to the reference genome of Termitomyces sp. J132 for haplotype reconstruction. After removal of the recombinant haplotypes shared between the heterokaryon and either homokaryons, we inferred that 5.04% of the haplotypes from the heterokaryon were the recombinants resulting from homologous recombination distributed genome-wide. With RNA transcripts of four meiosis-specific genes, including SPO11, DMC1, MSH4, and MLH1, detected from a mycelial sample by real-time quantitative PCR, the nuclear behavior in mycelia was reconfirmed meiotic-like. Conclusion: Unlike other basidiomycetes where sex is largely restricted to basidia, Termitomyces maximizes sexuality at somatic stage, resulting in an ever-changing genotype composed of a myriad of coexisting heterogeneous nuclei in a heterokaryon. Somatic meiotic-like recombination may endow Termitomyces with agility to cope with termite consumption by maximized genetic variability.

AB - Background: Termitomyces mushrooms are mutualistically associated with fungus-growing termites, which are widely considered to cultivate a monogenotypic Termitomyces symbiont within a colony. Termitomyces cultures isolated directly from termite colonies are heterokaryotic, likely through mating between compatible homokaryons. Results: After pairing homokaryons carrying different haplotypes at marker gene loci MIP and RCB from a Termitomyces fruiting body associated with Odontotermes formosanus, we observed nuclear fusion and division, which greatly resembled meiosis, during each hyphal cell division and conidial formation in the resulting heterokaryons. Surprisingly, nuclei in homokaryons also behaved similarly. To confirm if meiotic-like recombination occurred within mycelia, we constructed whole-genome sequencing libraries from mycelia of two homokaryons and a heterokaryon resulting from mating of the two homokaryons. Obtained reads were aligned to the reference genome of Termitomyces sp. J132 for haplotype reconstruction. After removal of the recombinant haplotypes shared between the heterokaryon and either homokaryons, we inferred that 5.04% of the haplotypes from the heterokaryon were the recombinants resulting from homologous recombination distributed genome-wide. With RNA transcripts of four meiosis-specific genes, including SPO11, DMC1, MSH4, and MLH1, detected from a mycelial sample by real-time quantitative PCR, the nuclear behavior in mycelia was reconfirmed meiotic-like. Conclusion: Unlike other basidiomycetes where sex is largely restricted to basidia, Termitomyces maximizes sexuality at somatic stage, resulting in an ever-changing genotype composed of a myriad of coexisting heterogeneous nuclei in a heterokaryon. Somatic meiotic-like recombination may endow Termitomyces with agility to cope with termite consumption by maximized genetic variability.

UR - http://www.scopus.com/inward/record.url?scp=85029755724&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85029755724&partnerID=8YFLogxK

U2 - 10.1186/s40529-017-0191-9

DO - 10.1186/s40529-017-0191-9

M3 - Article

VL - 58

JO - Botanical Studies

JF - Botanical Studies

SN - 1817-406X

IS - 1

M1 - 39

ER -