Scientia Agricultura Sinica ›› 2020, Vol. 53 ›› Issue (11): 2305-2320.doi: 10.3864/j.issn.0578-1752.2020.11.016

• RESEARCH NOTES • Previous Articles    

Diversity of Endophytic Fungi in Transgenic Rice Seeds from Different Planting Sites Based on PTN System

ZHAO Yan,WANG TianQi,ZHU JunLi   

  1. College of Food Science and Biotechnology, Zhejiang Gongshang University, Hangzhou 310018
  • Received:2019-10-09 Accepted:2020-02-18 Online:2020-06-01 Published:2020-06-09


【Objective】To provide scientific bases for study of the unintended variation in seed endophytic fungi community structure of genetically modified (GM) rice and explore the causing factors of variation, comparative analysis of the richness and biodiversity of seed endophytic fungi were conducted, using GM rice relative near-isogenic lines of different varieties in different cultivation sites as materials. 【Method】 Collect transgenic rice line which harboring the glyphosate resistant 2mG2-epsps gene (T) and its corresponding parent variety (P) and non-transgenic tissue culture regeneration control line (NR) to make parent control-transgenic plant line-non-transgenic control (PTN) near-isogenic line. The parent japonica rice Nipponbare (P1) and its corresponding transgenic line T23 and the NR control line NR18 formed the P1 near-isogenic line (P1L), the P2 near-isogenic line (P2L) composed of parent japonica rice PJ574 (P2) and its corresponding transgenic line T23 and the NR control line NR18. All rice samples were planted in two plantations including Hainan province (H) and Fuyang city of Zhejiang province (F) and the resulting seeds were harvested. The rice endophytic fungi were isolated by tissue separation method, strains were classified and identified with morphology and molecular biology methods. The isolation rate (IR), isolation frequency (IF), richness Margalef index (D), diversity Shannon-Wiener index (H') and Evenness index (E) were used to reflect the structure and distribution of rice seed endophytic fungi, and Sorenson similarity coefficient (Cs) and Fisher’s exact test were employed to describe the composition difference of endophytic fungi between rice samples. 【Result】A total of 121 endophytic fungi strains were isolated from rice seed samples of P1L and P2L near-isogenic lines that harvested in Hainan (H) and Zhejiang (F) plantations, they were identified as 15 genera, of which Curvularia, Dendryphiella, Epicoccum, Fusarium were confirmed as the dominant flora, with Fusarium as the common dominant genus of both H and F plantations. The total RF (4.61%) of endophytic fungi from Zhejiang-grown rice seeds is 5.05 times than that of Hainan-grown rice samples (0.83%). The richness Margalef index (D=2.29), Shannon-Wiener diversity index (H'=1.63) and Evenness index (E=0.66) of endophytic fungi flora from rice seeds in F plantation were higher than that (D=1.67, H'=0.63, E=0.29) of samples in H plantation. The seed endophytic fungi communities of P1L and P2L in H plantation had a similarity coefficient of 0.615, and that was 0.737 in F plantation, showing moderate similarity, and the Fisher’s exact test analysis suggested that there were no significant difference (P>0.05) between them. The GM lines except HT16 showed moderate similarity to their corresponding parent controls referring seed endophytic fungi communities, with similarity coefficient ranged between 0.500 and 0.667. But compared with their corresponding parents, the GM rice lines showed notably unintended variations in IF and genus numbers of endophytic fungi, the variation direction and amplitude of IF varied between different plantations. Also, the GM line FT16 increased 2 additional fungi genera Phaeosphaeria and Nigrospora, HT23 and FT23 respectively added 1 genus Letendraea helminthicola and 2 genera including Curvularia and Cladosporium. These genera increasing variations of endophytic fungi in GM rice seeds were derived from transgenic insertion mutation, whose safety needs to be focused on. While the genera decreasing variations of endophytic fungi in GM rice seeds were derived from somaclonal variation of tissue culture, which were safer. The variation amplitude order of total IF of rice endophytic fungi were as follows. Difference between H and F plantations referring to P1 and P2 (30.58%)>Difference between P1 and P2 varieties (27.28%)>Variation of NR lines (23.14%)>Variation of GM lines (22.32%). The genus number variations of rice endophytic fungi ranked as follows. Difference between H and F plantations referring to P1 and P2 (9)>Difference between P1 and P2 varieties (8) = Variation of NR lines (8) = Variation of GM lines (8). 【Conclusion】Rice seeds have abundant and diverse endophytic fungi, with majority of the culturable stains belong to Ascomycetes. Composition of rice seed endophytic fungi community shows geographical differences, and Fusarium is very common dominant genus in rice seeds grown both in Hainan and Zhejiang. The structure of endophytic fungi flora in rice seeds are affected by transgenic manipulation as well as tissue culture technology, while their unintended variation effects are less than that of rice growing locations and variety differences. The genera increasing variations of endophytic fungi in GM rice seeds are derived from transgenic insertion mutation, and the safety needs to be assessed.

Key words: transgenic rice seed, culturable endophytic fungi, unintended variation, PTN system, diversity

Fig. 1

Partial separation mapping of endophytic fungi from rice seeds a: Control; b, c, d, e: Colony separation diagram"

Fig. 2

Colony morphology of endophytic fungi from rice seeds on PDA plates Upper: Petri dish front; Bottom: Petri dish reverse side"

Table 1

Identification results of culturable endophytic fungi in rice seeds"





Compare similar species
Comparison result
WF6 Ascomycetes Pleosporales Pleosporaceae Curvularia Curvularia lunata strain S3-2 97 99 Curvularia lunata strain WF6 0.54
WF44 Curvularia lunata isolate E16 97 99 Curvularia lunata isolate WF44 0.08
合计Total 0.63
WF17 Pleosporales Pleosporales sp. strain APBSDSF36 97 100 Pleosporales sp. strain WF17 0.04
合计Total 0.04
WF22 Phaeosphaeria Phaeosphaeriopsis musae isolate DFFSCS029 99 99 Phaeosphaeriopsis musae strain WF22 0.04
WF55 Phaeosphaeria papayae isolate LQ122404 98 99 Phaeosphaeria papayae isolate WF55 0.04
合计Total 0.08
WF40 Setophoma Setophoma vernoniae strain CPC 23123 92 93 Setophoma vernoniae strain .WF40 0.13
合计Total 0.13
WF39 Ascomycetes Pleosporales Pleosporaceae Ophiosphaerella Ophiosphaerella agrostidis strain MFLUCC 11-0152 95 99 Ophiosphaerella agrostidis strain.WF39 0.13
WF58 Ophiosphaerella agrostidis isolate MFLUCC 16-0895 94 99 Ophiosphaerella agrostidis isolate WF58 0.04
合计Total 0.17
WF41 Dendryphiella Dendryphiella sp. crri.34 98 99 Dendryphiella sp. WF41 0.83
WF42 Dendryphiella sp. crri.34 97 99 Dendryphiella sp. WF42 0.75
WF45 Dendryphiella sp. crri.34 98 99 Dendryphiella sp.WF45 0.08
WF46 Dendryphiella sp. crri.34 98 99 Dendryphiella sp.WF46 0.08
WF59 Dendryphiella sp. crri.34 98 99 Dendryphiella sp. WF59 0.13
合计Total 1.88
WF48 Bipolaris Bipolaris oryzae isolate BO1 97 99 Bipolaris oryzae isolate WF48 0.04
WF62 Bipolaris sorokiniana strain A0606 95 97 Bipolaris sorokiniana strain WF62 0.04
合计Total 0.08
WF49 Pithomyces Leptosphaerulina chartarum strain DH08111quan1 98 99 Leptosphaerulina chartarum strain WF49 0.04
合计Total 0.04
WF43 Didymellaceae Epicoccum Epicoccum sorghinum strain BJ-F1 97 99 Epicoccum sorghinum strain.WF43 0.08
WF47 Epicoccum sorghinum isolate M3 98 99 Epicoccum sorghinum isolate WF47 0.13
WF52 Epicoccum sorghinum isolate M3 97 99 Epicoccum sorghinum isolate WF52 0.38
WF53 Epicoccum sorghinum isolate M3 96 99 Epicoccum sorghinum isolate WF53 0.04
合计Total 0.63
WF51 Leptosphaeriaceae Leptosphaeria Leptosphaeria sp. SL14 99 99 Leptosphaeria sp. WF51 0.04
WF61 Leptosphaeria sp. isolate LQ122416 98 99 Leptosphaeria sp. isolate WF61 0.04
WF64 Leptosphaeria sp. isolate LQ122417 98 99 Leptosphaeria sp. isolate WF64 0.04
合计Total 0.13
WF20 Moniliales Dematiaceae Nigrospora Nigrospora sp. JL4-CGL24 99 99 Nigrospora sp. WF20 0.04
WF57 Nigrospora sp. HCH267 98 99 Nigrospora sp. WF57 0.04
WF60 Nigrospora oryzae strain APBSMLF76 98 99 Nigrospora oryzae strain WF60 0.04
合计Total 0.13
WF3 Cladosporium Cladosporium oxysporum isolate DFFSCS018 100 99 Cladosporium sp. WF3 0.04
WF19 Cladosporium oxysporum strain SCAU101 99 99 Cladosporium oxysporum strain WF19 0.04
WF63 Cladosporium xanthochromaticum 98 99 Cladosporium xanthochromaticum WF63 0.08
WF65 Cladosporium tenuissimum strain APBSDSF6 99 99 Cladosporium tenuissimum strain WF65 0.04
合计Total 0.21
WF4 Alternaria Alternaria sp. H6_E08_1104035148Q 100 99 Alternaria sp.WF4 0.04
WF18 Alternaria alternata strain EN24 98 100 Alternaria alternata strain WF18 0.04
WF31 Alternaria longissima strain CLB44 98 99 Alternaria longissima strain WF31 0.04
合计Total 0.13
WF9 Tuberculariaceae Fusarium Fusarium chlamydosporum NBAIM:236 98 100 Fusarium chlamydosporum strain WF9 0.04
WF14 Fusarium chlamydosporum isolate LrSF22 99 99 Fusarium chlamydosporum strain WF14 0.04
WF15 Fusarium sp.
AL-14 IRH-2012a
98 99 Fusarium sp. WF15 0.04
WF16 Fusarium equiseti strain CP16 99 99 Fusarium equiseti strain WF16 0.04
WF38 Fusarium sp. Z13-09 96 99 Fusarium sp.WF38 0.08
WF50 Fusarium sp.
AL-15 IRH-2012b
98 99 Fusarium sp.WF50 0.38
WF54 Fusarium proliferatum isolate MC-23-F 99 99 Fusarium proliferatum isolate WF54 0.04
WF56 Fusarium proliferatum isolate 10R-7 98 99 Fusarium proliferatum isolate WF56 0.04
WF66 Fusarium proliferatum isolate LrBF18 99 99 Fusarium proliferatum isolate WF66 0.04
合计Total 0.75
WF23 Fungi Imperfecti Hypocreales Hypocreaceae Letendraea helminthicola Letendraea helminthicola strain B1A0062SNA2CC1081 88 100 Letendraea helminthicola strain WF23 0.04
合计Total 0.04
总分离率Total IR(%) 5.04

Table 2

Comparison of isolation frequency (IF) (%) of endophytic fungi in rice seeds from different planting sites (%)"

海南省Hainan (H) 浙江省富阳市Fuyang, Zhejiang (F)
HP1 HT16 HNR25 HP2 HT23 HNR18 FP1 FT16 FNR25 FP2 FT23 FNR18
Curvularia 1.65 1.65 0.83 5.79 2.48
Pleosporales 0.83
Phaeosphaeria 0.83 0.83
Setophoma 1.65 0.83
Ophiosphaerella 2.48 0.83
Dendryphiella 12.40 5.79 8.26 3.31 0.83 6.61
Bipolaris 0.83 0.83
Pithomyces 0.83
Epicoccum 3.31 1.65 0.83 0.83 4.96 0.83
Leptosphaeria 0.83 0.83 0.83
Nigrospora 0.83 0.83 0.83
Cladosporium 0.83 0.83 2.48
Alternaria 0.83 0.83 0.83
Fusarium 1.65 0.83 0.83 3.31 4.13 1.65 1.65 0.83
Letendraea helminthicola 0.83
Sum of IF
0.00 5.79 1.65 4.96 2.48 1.65 30.58 14.05 9.09 8.26 13.22 8.26
7.44 9.09 53.72 29.75
16.53 83.47

Table 3

The endophytic fungal diversity indexes of rice seeds from PTN near-isogenic lines in Hainan (H) and Fuyang, Zhejiang (F) cultivation sites"

海南省Hainan (H) 浙江省富阳市Fuyang, Zhejiang (F)
No. of
No. of
index (D)
index (E)
No. of
No. of
index (D)
Index (H')
index (E)
P1 0 0 37 9 1.92 1.32 0.60
T16 7 5 1.82 1.40 0.87 17 6 1.20 0.74 0.41
NR25 2 1 0.00 0.33 11 2 0.24 0.35 0.51
P1L 9 6 1.67 1.14 0.64 65 11 2.17 1.35 0.56
P2 6 5 1.67 1.18 0.73 10 6 1.40 0.80 0.45
T23 3 3 0.83 0.65 0.60 16 6 1.40 1.07 0.60
NR18 2 2 0.42 0.44 0.63 10 3 0.56 0.53 0.49
P2L 11 7 0.30 1.34 0.69 36 8 1.52 0.99 0.48
合计Tatol 20 9 1.67 0.63 0.29 101 12 2.29 1.63 0.66

Table 4

Similarity coefficients (Cs) of endophytic fungi of rice seeds from PTN near-isogenic line samples in different cultivation places"

海南省Hainan (H) 浙江省富阳市Fuyang, Zhejiang (F)
P1 T16 NR25 P2 T23 NR18 P1 T16 NR25 P2 T23 NR18
P1 1.00 1.00
T16 0.00 1.00 0.53 1.00
NR25 0.00 0.00 1.00 0.36 0.50 1.00
P2 0.00 1.00 0.67 1.00
T23 0.50 1.00 0.67 1.00
NR18 0.29 0.00 1.00 0.67 0.67 1.00
P1L 0.62 0.74
H 0.57

Table 5

Analysis the differences (P) composition of endophytic fungi of rice seeds from PTN near-isogenic line samples in different cultivation places "

海南省Hainan (H) 浙江省富阳市Fuyang, Zhejiang (F)
P1 T16 NR25 P2 T23 NR18 P1 T16 NR25 P2 T23 NR18
P1 1.00 1.00
T16 1.00 0.23 1.00
NR25 0.09 1.00 0.38 0.07 1.00
P2 1.00 0.33 1.00
T23 1.00 1.00 0.05 1.00
NR18 0.86 1.00 1.00 0.61 0.00 1.00
P1L 0.86 0.18
H 0.00

Fig. 3

Relative isolation frequency ( RF ) of endophytic fungi from rice seeds grown in Hainan (H) and Fuyang, Zhejiang (F) "

Fig. 4

The cluster analysis of endophytic fungi composition of rice seeds from the 6 samples planted in Hainan (H) and Fuyang, Zhejiang (F) "

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