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Mycorrhizal fungi in the waiting room: fungal associations in Orchidaceae shed light on mycorrhizal evolution

Authors:

Abstract

Research commentary about the paper: Selosse MA, Petrolli R, Mujica MI, et al. 2022. The Waiting Room Hypothesis revisited by orchids: were orchid mycorrhizal fungi recruited among root endophytes? Ann Bot 129:259–270. https://doi.org/10.1093/aob/mcab134.
Mycorrhizal fungi in the waiting room: fungal associations in
Mycorrhizal fungi in the waiting room: fungal associations in
Orchidaceae shed light on mycorrhizal evolution.
Orchidaceae shed light on mycorrhizal evolution.
María Isabel Mujica1, 2* and Marc-André Selosse3, 4, 5
1Institute of Environmental and Evolutionary Science, Universidad Austral de Chile, Chile. 2Center for
Chilean Orchids Conservation (Cecorch), Chile. 3Institut de Systématique, Évolution, Biodiversité,
Muséum national d’Histoire naturelle, Sorbonne Universités, France. 4Department of Plant Taxonomy
and Nature Conservation, University of Gdańsk, Poland. 5Institut Universitaire de France, France.
*E-mail: ((,E'B,'"'
) 5 " () # ) " ,7 5
(7'"A,))".,)5
5,)# (7'"A "-  )) "
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"7#)7 K:" et al &L )
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5,)# .7 .. 5( -'
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5( 5,)# "7#)(' K:" et al
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". ).. . #)(' (M')
"  -. ' )# 5
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)A7( ')# ) #)) ) ', )
" .M') 5 ). )#8'M'
7(-8),' #) K!7,'" et al
L
')7 )" ') 5 " .,)
55,)#(7'"A57/,##
-7"P>)#(;7"QK>;L"
"7" , " ) ()7 '
(7'"A "- (#" ". .. 5(
 )"7( !7'"A ')
(7 5 -" ) KL ("#'
(M')KL  -, " (7'"A )
KL ( - ) )) ),)
1'")# ") ) )"7( " >;
")"7i.e.5,)#"
')A  )  ) )
("#' 7(( ) N))
5 )  " " ) K#,A et al
*L    -'(
(7'"A)'"7'',7)'#'
)'" " / " ))  #"
') /" " " I/)# "
"7"  )"7( '  
7(-' _/)# (\ /" -"'
'1)'  .,) /
(,,( /"  ( '(1 E)
(7'"A ("#) K et al
TL
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5 " .,)7 )) 
(7'"A , '', " 5,)#, "
 )/ (7'"A )  #.) ) )#
(7 ". ) )"7' - )
" ) )# ) ", "  ,
)'" " )"7' )'  '7
1' ) ) "7#)'7 ' 
" ) "  (7'"A ') #.)
""(7'"A"-1'-
.  " (7'"A )# 
"7#)'7 ()# 8.#)#
)#")"7'")"
-) -. 5 1( ) "
-')/"'"7..'"
'(7'"A ) ' (7'"A
"-5()"7')'K>jet al
 L  '', ) ( -' ' 5
"#),Mycena/"'"<)/)-
)"7' )  '',  (7'"A
5,)# ) '" K et al L  )
'' KH et al $L )  ')
' ,-" ) Ann Bot K  
L/1()"5,)#'))
'"' 5( ) .,)7
'.)">;
IMS Newsletter - 22
'" -)#  %# /"'" 5(
-,', (7'"A /" H((7'
K(" )  TL ;/. (
'" )',)# " ( )')7
.#)# )# ' /"
"A')87"7'#,5(-7
" -(7', 5(
)' -' )
,)' KD)7 et al L "
,## " "  '(() )' 5
1)'"/--7(7'"A/"
"A')  /  , -7 "
'),')5)'K>)#et al
L ", '" -))
H((7') ) "5  
(7'"A')/""A')
 -)# (7'"A "A') 
58.)#  - " '(
#)' (  "7 ". -) "/) 
#/ ) ) '7)# ( K(" )
 TL ) ". # )A7('
"- K!7,'" et al L + "7 
 )"7 ) ))8'" )^ I
1( Serendipita (= Pyriformospora) indica
  /8, ( 5 ) )"7
"'"(7'"A!(-5
,)'  )"7' # )
Euphorbia  ) Bromus erectus )
",#" ()7 -' 
' ) ))8'"  ( '
 7(( ) )"7' K
5)' )  et al L ",
"A')  -' ) )"7' )
))8'"  % 1' ,) "
>; " (. '#7 (7 - 
)  .. (7'"A -
) )7 ) " )' 5 '" -, 
) " ) #, ) (
"A') )# /  ', )
" (7'"A 7 '(7'"A
')  ) " " 5( 5
"A') ) ((- 5
)'/','
(7'"A 5,)# K 5)' ) >j et
al   )  et al L ",
)"7( ) "A') <7 /
"))'(7'"A)'8
5()# (7'"A K'" ) '
(7'"AL1'-7">;
 " ') /" "A')
( '" ' ". "5 )
5("A')'(7'"A5,)#
IMS Newsletter - 23
,-7
Daniela Aros-Mualin
Daniela Aros-Mualin
" 7(- /" " )/ ) 
)<  " "7#' -7  1'
'-)'(,)5("5,)#,(5
" '" , " 5,)#, ) 1',.
'-) ,' )  "5
(7'""' /" " ,
5,)# '-) ) )  ,"7
<)/)  (1"' '" K(" )
 TO D)7 et al L ,'"
)) 5 ) ) ),)
"7#7 '', ').#)7 ) '"
.,) K>)# et al. L ))#7
'(7'"A5,)#5S,)7'
 / 5S,)' )  5 5,7
"7)"'"A')8''"
K)   &? ' ",#", "
"7#)7 5 " '" 5(7 - ) ?
,O  -  )  et al L
=--7 " 1  ) 
)"7 /"'"  , -7 "
#/)# .)' " ( '(7'"A
5,)# ')A "  5 ))8
'(7'"A )  )"7
K et al TL " )' 5 "
5,)#  )"7 ) )' #)
'" )  (7'"A ) . ))8
5,7 ,"' )#  ' -7 "
>;
I)7 "  ( '" " "5
5( "A')  -' 5,)# 
' /" " )) 
(7'""7</"-./"
'(7'"A5,)#-'5,)#
)  / 5S,)' )  5
"A')8' #) '" K) 
&'",#",""7#)75
" '" 5(7 - ) & ,O 
-  )  et al L ) -" '
'(7'"A ) -' 5,)# )
 )"7 )  5 #) '" 
.-8)"/)#(8-',
..(7'"A)')1'
,)">;
 et al KL '( .)' "
, " "7" " " .
'" (7'"A ') K5( "
)' "A')  " ., .
5,)# )L  - ) "
.,)7 ',() 5 )"7 "
-'( (7'"A 5/)# " >; "
/)#("7" )"5'5
) '',(,. .)' 5 , )'" )
5,)# ' / -7 " )')#
)"/"5,)#'((,)
' )  ", / -. " "
) ) '-)# ('- .7
( '(").7 / . )/
.)'  5,"  " )# 5
')5"/)#("7"
References
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8 D)7 9D> ! I  !%  '" (7'"A
(', '#7 "7#7 .,) ) ').) '
) Fungal Associations ) O ;'<  KL " !7' W )
)#=$8"@@#@$@*$T88 ?8T 8C
8HH8%H<DI;,)H9et al$%)#/"8
()# 7(- -/) Mycena galopus ) Vaccinium
corymbosum)#Mycorrhiza$T8T*
"@@#@$@&$8$8$*$8&
8 :" % :, % #7 H et al & ).#)5 '7
('")( )  ,). 5 7(- #) ) (7'"A
(,,Nat Genet?$?8?&"@@#@T@)#
8)7!7,'"!)et al.,)7))
"'(7'"A"-)"#)(5"7.)#
5(,"(85()#5,)#New Phytol*?8*
"@@#@@)"$T*
8 !7,'"  :  :, % et al  #8' #)(
S,)')# 5 (7'"A 5,)# . )#" ) " 7
.,)57(-'Nat Commun&&
"@@#@T@?? $88T$*&8/
8  !% ! I =7  et al  "' 5,)#
7(-) ) ' '""7, '" Plant Signal Behav
&?*8&"@@#@? @-&?$*
8  !% '")8!,),7  ! I T (  8
")<5,)#'#7U I,)# '#')'" 5)E,#
New Phytol$* T8*$"@@#@@)"?*T
8  !% =  !,E' ! et al  " >)# (
;7" . -7 '" / '" (7'"A 5,)#
',()#)"7UAnn Bot*&*4$
"@@#@*@-@('-?
8 ("   D9 T !7'"A 7(- (-#
.
8>)#D9'S,(7); H(I et al7(-)/'")#
)"'("5)'"'New Phytol$*8T
"@@#@@)"$??
8>j !>IJ,'' % !8%  -') 4)
",) ) ) )') /" ) ) New Phytol 8
?"@@#@@)"*$$
IMS Newsletter - 24
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Root endophytism and mycorrhizal associations are complex derived traits in fungi that shape plant physiology. Sebacinales (Agaricomycetes, Basidiomycota) display highly diverse interactions with plants. Although early‐diverging Sebacinales lineages are root endophytes and/or have saprotrophic abilities, several more derived clades harbour obligate biotrophs forming mycorrhizal associations. Sebacinales thus display transitions from saprotrophy to endophytism and to mycorrhizal nutrition within one fungal order. This review discusses the genomic traits possibly associated with these transitions. We also show how molecular ecology revealed the hyperdiversity of Sebacinales and their evolutionary diversification into two sister families: Sebacinaceae encompasses mainly ectomycorrhizal and early‐diverging saprotrophic species; the second family includes endophytes and lineages that repeatedly evolved ericoid, orchid and ectomycorrhizal abilities. We propose the name Serendipitaceae for this family and, within it, we transfer to the genus Serendipita the endophytic cultivable species Piriformospora indica and P. williamsii . Such cultivable Serendipitaceae species provide excellent models for root endophytism, especially because of available genomes, genetic tractability, and broad host plant range including important crop plants and the model plant Arabidopsis thaliana . We review insights gained with endophytic Serendipitaceae species into the molecular mechanisms of endophytism and of beneficial effects on host plants, including enhanced resistance to abiotic and pathogen stress. Contents Summary 20 I. Introduction 21 II. Phylogeny and systematics of Sebacinales 21 III. Ecology and diversity of Sebacinales interactions with plants 23 IV. Endophytism in Serendipitaceae: changing phenotype of the host plants 29 V. Endophytism in Serendipitaceae: a fungal adaptation to biotrophy 33 VI. Conclusion and future directions 35 Acknowledgements 36 Author contributions 36 References 36
Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom-forming fungi
  • A Kohler
  • A Kuo
  • L G Nagy
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