Insight into vital role of autophagy in sustaining biological control potential of fungal pathogens against pest insects and nematodes

Figures & data

Table 1. Autophagy-related proteins (ATGs) found in the NCBI protein databases of yeasts, fungal entomopathogens and nematophagous fungi.

ATG	NCBI accession codes*
	Hp	Kp	Kph	Sc	Aal	Aap	Bba	Bbr	Cm	If	Ll	Mac	Man	Mr	Nr	Sp	Aol	Hm
1	ESW98768	ANZ75424	CAY69285	P53104	OAA32035	KZZ98101	EJP64020	OAA47468	ATY62103	OAA71303	OAA80090	EFY88904	KJK76758	EFZ00905	OAA44768	OAA58087	EGX50159	KJZ72849
2	ESW96436	ANZ73551	CAY67230	P53855	OAA33259	KZZ92259	EJP62566	OAA39029	ATY66591	OAA53106	OAA80419	EFY85935	KJK76344	EFZ01946	OAA39436	OAA59125	EGX44288	KJZ72057
3	ESW97715	ANZ76765	CAY70737	P40344	KZZ95324	KZZ96434	EJP63325	OAA38715	ATY61762	OAA60125	OAA75012	EFY88596	KJK75521	EFZ01113	OAA44978	OAA63351	EGX49425	KJZ79335
4	ESW98784	ANZ76419	CAY68374	P53867	KZZ93420	KZZ90947	EJP61110	OAA34578	ATY64819	OAA73766	OAA81896	EFY93633	KJK84136	EFY99546	OAA49518	OAA54482	EGX47408	KJZ70398
5	ESW99543	ANZ77851	CAY71712	Q12380	OAA33555	KZZ87486	EJP62801	OAA52240	ATY61495	OAA60740	OAA76966	EFY90145	EFY90145	EXU96089	OAA42093	OAA62418	EGX50306	KJZ79622
6	ESW98526	ANZ77485	CAY68819	Q02948	KZZ92081	KZZ91922	EJP69800	OAA40746	ATY65156	OAA68923	OAA81116	EFY86689	KJK79721	KHO11008	OAA46931	OAA68176	EGX49628	KJZ77316
7	ESW98216	ANZ74180	CAY68151	P38862	OAA33422	KZZ95791	EJP62461	OAA51370	ATY66145	OAA63006	OAA70982	EFY91403	KJK76449	EFZ01845	OAA42261	OAA68507	EGX45886	KJZ73174
8	ESW99851	ANZ77907	CAY71966	P38182	OAA33691	KZZ97062	EJP69267	OAA37148	ATY67476	OAA58875	OAA76358	EFY85199	KJK82117	EFZ01445	OAA46238	OAA55906	EGX52603	KJZ72025
9	ESW96528	ANZ77553	CAY71765	Q12142	KZZ93426	KZZ90329	EJP61034	OAA34570	ATY64768	OAA73774	OAA81888	EFY93626	KJK84144	EFY99555	OAA49525	OAA54510	EGX51301	KJZ70407
10	ESW98616	ANZ75463	CAY70737	Q07879	KZZ97664	–	EJP70966	OAA45929	EGX89933	OAA73685	OAA81814	EFY90956	KJK73827	OAA48754	OAA48754	OAA59012	EGX50380	KJZ78386
11	ESX02153	ANZ76715	CAY68411	Q12527	OAA32739	KZZ88894	EJP66943	OAA48105	ATY61095	OAA67574	OAA77977	EFY90855	KJK78949	EFZ00535	OAA42617	OAA53787	EGX54268	KJZ73499
12	ESW96997	ANZ74286	CAY70406	P38316	KZZ96701	KZZ95708	EJP64666	OAA46448	ATY67028	OAA63828	OAA74290	EFY91312	KJK81831	EFZ02238	OAA51680	OAA62640	EGX43872	KJZ75788
13	ESW98330	ANZ75343	CAY69477	Q06628	KZZ91450	KZZ87338	EJP67952	OAA42381	EGX93111	OAA70524	OAA79351	EFY90437	KJK83836	EFZ02694	OAA50594	OAA68682	EGX43338	KJZ73196
14	–	–	–	P38270	–	–	–	–	–	–	–	–	–	–	–	–	–	–
15	ESW99625	ANZ73852	CAY67386	P25641	KZZ90734	KZZ90664	EJP62335	OAA38950	ATY58944	OAA58221	OAA80311	EFY87240	KJK79485	EFZ03432	OAA34412	OAA64287	EGX46578	KJZ73386
16	ESW98669	ANZ75755	CAY71305	Q03818	KZZ93856	–	EJP66477	OAA49178	ATY61736	OAA64011	OAA79801	–	KJK79436	EFY95610	OAA38355	OAA67064	EGX51377	KJZ74754
17	ESX00887	ANZ76024	CAY69318	Q06410	KZZ91807	KZZ87046	EJP62668	OAA46696	ATY58611	OAA53674	OAA71841	EFY87591	KJK78562	EFY97482	OAA50385	OAA56219	EGX51841	KJZ76468
18	ESX02211	ANZ76366	CAY70991	P43601	KZZ94876	KZZ89532	EJP61015	OAA36986	ATY67510	OAA58836	OAA76320	EFY84843	KJK83381	EFY99242	OAA44358	OAA59674	EGX53695	KJZ78877
19	–	–	–	P35193	–	–	–	–	–	–	–		–	–	–	–	–	–
20	ESW96614	ANZ76112	CAY69906	Q07528	OAA33120	KZZ95709	EJP66835	OAA48003	ATY60813	OAA74127	OAA74633	EFY90783	KJK77643	EFY98676	OAA43098	OAA53836	EGX43058	KJZ78961
21	ESX00158	ANZ76928	CAY71077	Q02887	OAA32982	KZZ92688	EJP65675	OAA52473	EGX91053	OAA54904	OAA79214	EFY89511	KJK75180	EFY94238	OAA36058	OAA60246	EGX45948	KJZ75213
22a	ESW98143	ANZ73516	CAY67729	P25568	KZZ89441	KZZ90658	EJP69073	OAA42939	ATY62792	OAA64972	OAA79970	EFY89712	KJK77771	EFY97213	OAA45553	OAA53950	EGX47846	KJZ76598
22b	–	–	–	–	KZZ96617	KZZ87966	EJP65688	OAA52486	ATY58739	OAA54918	OAA79201	EFY93887	KJK77427	EFY98889	OAA40064	–	–	KJZ75201
22c	–	–	–	–	–	–	EJP65315	OAA52574	ATY66541	OAA59477	OAA74415	EFY85468	KJK75171	EFY96161	OAA38895	–	–	–
22d	–	–	–	–	–	–	EJP61453	–	–	–	–	–	–	–	–	–	–	–
23	–	–	–	Q06671	–	–	–	–	–	–	–	–	–	–	–	–	–	–
24	ESW97141	ANZ75401	CAY69011	P47057	OAA32216	KZZ95709	EJP61354	OAA47182	ATY61719	OAA71568	OAA64158	EFY91127	KJK79963	EFY99206	OAA40571	OAA63756	EGX43379	KJZ78598
25	ESW97416	–	–	–	–	–	–	–	–	–	–	–	–	–	–	–	–	–
26	ESW96191	ANZ76118	CAY71393	Q06321	KZZ90874	KZZ92672	EJP71037	OAA45995	ATY62412	OAA73722	OAA81945	EFY86996	KJK79229	EFY97936	OAA36440	OAA59786	EGX51249	KJZ73456
27	ESW97460	ANZ75892	CAY69817	P46989	KZZ98281	KZZ88672	EJP63614	OAA44065	EGX88907	OAA52851	OAA76046	EFY88154	KJK81470	EFZ02138	OAA41305	OAA57639	EGX46770	KJZ73136
28	ESW99680	ANZ74931	CAY69233	–	KZZ89898	KZZ88029	EJP70908	OAA45872	EGX91880	OAA73420	OAA82283	EFY91502	KJK77990	EFY97624	OAA52097	OAA62786	EGX54013	KJZ75402
29	–	–	–	Q12092	KZZ98964	KZZ91602	EJP65671	OAA52469	EGX91048	OAA54900	OAA79218	EFY87305	KJK75147	EFY96138	OAA40057	OAA53661	EGX48917	KJZ75209
30	ESX03003	ANZ76622	CAY70917	–	–	–	–	–	–	–	–	–	–	–	–	–	–	–
31	–	–	–	Q12421	–	–	–	–	–	–	–	–	–	–	–	–	–	–
32	–	–	–	P40458	–	–	–	–	–	–	–	–	–	–	–	–	–	–
33	ESW96153	–	–	Q06485	OAA33167	KZZ86925	MH427003	OAA37283	EGX92109	OAA73257	OAA82461	EFY90900	KJK79096	EFZ00391	OAA48699	OAA65672	EGX49467	KJZ78329
34	–	–	–	Q12292	–	–	–	–	–	–	–	–	–	–	–	–	–	–
35	ESW99702	ANZ73929	CAY67399	Q06834	OAA33190	KZZ89124	EJP70174	OAA49997	ATY67046	OAA67449	OAA78001	EFY87220	KJK77556	EFY98763	OAA38060	OAA54133	EGX52149	KJZ78899
36	–	–	–	P46983	–	–	–	–	–	–	–	–	–	–	–	–	–	–
37	ESW98758	ANZ77961	CAY71862	–	KZZ98481	KZZ98004	EJP65590	OAA52386	ATY66944	OAA59434	OAA74461	EFY86719	KJK80967	EFY95727	OAA35690	OAA64419	EGX43362	KJZ80366
38	–	–	–	Q05789	–	–	–	–	–	–	–	–	–	–	–	–	–	–
39	–	–	–	Q06159	–	–	–	–	–	–	–	–	–	–	–	–	–	–
40	–	–	–	Q99325	–	–	–	–	–	–	–	–	–	–	–	–	–	–
41	–	–	–	Q12048	–	–	–	–	–	–	–		–	–	–	–	–	–
42	ESX02688	ANZ76773	CAY70682	P38109	OAA33069	KZZ88266	EJP62646	OAA46680	EGX91700	OAA53688	OAA71860	EFY87773	KJK77692	EFY98627	OAA43147	OAA58390	EGX53766	KJZ79011

* Found in the NCBI protein databases of four yeasts (Hp: Hansenula polymorpha DL1; Kp: Komagataella pastoris NRRL Y-1603; Kph: K. phaffii GS115; Sc: S. cerevisiae S288C), 12 entomopathogenic fungi (Aal: Aschersonia aleyrodis RCEF 2490; Aap: Ascosphaera apis ARSEF 7405; Bba: Beauveria bassiana ARSEF 2860; Bbr: B. brongniartii RCEF 3172; Cm: Cordyceps militaris CM01; If: Isaria fumosorosea ARSEF 2679; Ll: Lecanicillium lecanii RCEF 1005; Mac: Metarhizium acridum CQMa102; Man: M. anisopliae BRIP 53293; Mr: M. robertsii ARSEF 23; Nr, Nomuraea rileyi RCEF 4871; Sp: Sporothrix insectorum RCEF 264), and two nematophagous fungi (Aol: A. oligospora ATCC 24927; Hm: Hirsutella minnesotensis 3608). Red items are the ATGs that have been characterized in insect and nematode mycopathogens.

Figure 1. Autophagy-related (ATG) genes functioning in unicellular fungi. Forty-two ATG genes plus Vps14 and Vps34 involved in autophagy pathway of yeast species are sorted into two groups, of which one works in the “core” autophagy machinery and another participates in various specific pathways [24].

Figure 2. Overview of autophagic events in entomopathogenic and nematophagous fungi. (A) Divergent roles of autophagic events in sustaining the in vitro and in vivo cellular processes of B. bassiana, M. robertsii and A. oligospora, three representative mycopathogens that have evolved for adaptation to distinct host spectra and associated habitats and fall into different lineages. Autophagy mediates the asterisked process that is distinct for each of the fungal pathogens to penetrate through the host cuticle after conidial germination. (B) Transmission electronic microscopic images (scale bars: 0.2 μm) for intravacuolar autophagic events altered by singular deletions of ATG1, ATG5, ATG8 and ATG11 in B. bassiana. (C) Proposed model for autophagy pathways in B. bassiana, including starvation-induced or non-selective autophagy, selective autophagy and bulk autophagy. PE: phosphatidylethanolamine.

Yang Z, Huang J, Geng J, et al. Atg22 Recycles amino acids to link the degradative and recycling functions of autophagy. Mol Biol Cell. 2006;17(12):5094–5104.

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