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Acta Agronomica Sinica ›› 2023, Vol. 49 ›› Issue (6): 1466-1479.doi: 10.3724/SP.J.1006.2023.22039

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Ubiquitin receptor protein OsDSK2b plays a negative role in rice leaf blast resistance and osmotic stress tolerance

DING Jie-Rong1,**(), MA Ya-Mei1,**(), PAN Fa-Zhi2, JIANG Li-Qun1, HUANG Wen-Jie3, SUN Bing-Rui1, ZHANG Jing1, LYU Shu-Wei1, MAO Xing-Xue1, YU Hang1, LI Chen1,*(), LIU Qing1,*()   

  1. 1Rice Research Institute, Guangdong Academy of Agricultural Sciences/Guangdong Key Laboratory of New Technology in Rice Breeding/Guangdong Rice Engineering Laboratory, Guangzhou 510640, Guangdong, China
    2South China Agricultural University, Guangzhou 510642, Guangdong, China
    3Agro-biological Gene Research Center, Guangdong Academy of Agricultural Sciences/Guangdong Key Laboratory for Crop Germplasm Resources Preservation and Utilization, Guangzhou 510640, Guangdong, China
  • Received:2022-06-22 Accepted:2022-11-25 Online:2023-06-12 Published:2022-12-07
  • Contact: *E-mail: liuqing198504@126.com;E-mail: 2369538973@qq.com
  • About author:First author contact:**Contributed equally to this work
  • Supported by:
    Investment Project of Department of Agriculture and Rural Affairs, Development and Reform Commission, Guangdong province(Yue Fa Gai Nong Jing [2021]272);Special Fund for Scientific Innovation Strategy-Construction of High Level Academy of Agriculture Science(R2020PY-JX001);Guangdong Key Laboratory of New Technology in Rice Breeding(2020B1212060047)

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Abstract:

The ubiquitin receptor protein DSK2 (dominant suppressor of KAR2) plays an important role in the growth, development, and stress tolerance in plant, but its role in rice disease resistance and osmotic stress has not been reported yet. In this study, we identified that OsDSK2b was regulated by various stresses, and the relative expression level of this gene decreased significantly after Magnaporthe oryzae infection and 20% PEG-6000 treatment. The spatio-temporal expression analysis showed that the relative expression level of OsDSK2b was highest at three-leaf seedling stage. The subcellular localization analysis demonstrated that OsDSK2b was localized in the cytoplasm in rice protoplast. The lesion area of OsDSK2b knockout plants was about 0.05 cm2 and 0.10-0.13 cm2, which was much smaller than wild-type plants (0.24 cm2 and 0.31 cm2) after inoculation with Magnaporthe oryzae (GD08-T13 and Guy11). Compared with wild-type plants, knockout of OsDSK2b significantly enhanced the leaf blast resistance in rice, and the relative expression levels of pathogenesis-related protein (PR) genes were induced significantly in OsDSK2b knockout plants after Magnaporthe oryzae (Guy11) infection. The knockout of OsDSK2b also significantly enhanced the osmotic stress tolerance in rice. OsDSK2b knockout plants had higher survival rate (58.3%-74.0%) than wild-type plants (17.0%) after 20% PEG-6000 treatment. Meanwhile, compared with wild-type plants, OsDSK2b knockout plants had lower ion permeability and water loss rate after 20% PEG-6000 treatment. Scanning microscopy revealed that knockout of OsDSK2b could promote the stomatal closure both before and after 20% PEG-6000 treatment, and the promotion effect was stronger after osmotic stress treatment. In addition, qRT-PCR results showed that the relative expression level of DREB genes and abscisic acid (ABA) synthesis or pathway-related genes were significantly higher in OsDSK2b knockout plants than wild-type plants after osmotic stress treatment. The endogenous ABA contents of ko6 and ko14 knockout plants were 314.2 ng g-1 and 344.4 ng g-1, respectively, which were significantly higher than wild-type plants (206.8 ng g-1). These results indicated that OsDSK2b could regulate rice osmotic stress through both the ABA-dependent and ABA-independent pathways. This study provides a new candidate gene for the breeding of rice resistant varieties by analyzing the regulatory role of OsDSK2b in rice coping with biotic and abiotic stresses.

Key words: rice (Oryza sativa L.), rice blast, osmitic stress, PR, DREB, ABA

Table 1

Primers used for vector construction and qRT-PCR"

引物名称
Primer name		 引物序列
Primer sequence (5°−3°)
OsDSK2b-6a-F/R TTGGTTGGTTAGAACCCTGACGGCAGCCAAGCCAGCA/TCAGGGTTCTAACCAACCAAGTTTTAGAGCTAGAAAT
OsDSK2b-6b-F/R CTGCTAGGAGCAGCTGAAGCAACACAAGCGGCAGC/CTTCAGCTGCTCCTAGCAGGTTTTAGAGCTAGAAAT
Pps-GGL/Pgs-GG2 TTCAGAGGTCTCTCTCGACTAGTATGGAATCGGCAGCAAAGG/AGCGTGGGTCTCGTCAGGGTCCATCCACTCCAAGCTC
Pps-GG2/Pgs-GGR TTCAGAGGTCTCTCTGACACTGGAATCGGCAGCAAAGG/AGCGTGGGTCTCGACCGACGCGTATCCATCCACTCCAAGCTC
U-F/gR-R CTCCGTTTTACCTGTGGAATCG/CGGAGGAAAATTCCATCCAC
SP1/SP2 CCCGACATAGATGCAATAACTTC/GCGCGGTGTCATCTATGTTACT
OsDSK2bJC-F/R TCTTTTCTTGCTTCTCACACTCC/TTGCCAGTAGAACCTGCCCG
OsDSK2b-F/R TGGTAGCCAAGGAGGCAATG/ATTGCCAAGAAGACGCTCCA
PR1a-F/R CGTCTTCATCACCTGCAACTACTC/CATGCATAAACACGTAGCATAGCA
PR2-F/R CCTTCACCAAGTATCTGCGA/GTCTAGCGCATTCTGCAAAC
PR5-F/R ACGAAATACTCCAAGTTCTTCAAGG/GTAATTTGTTCCGGCAGGGC
PR8-F/R TCTACGACGTGCAGAACAACTTCAG/TCCAACTCAACCACTGTGCAAGTAA
PR10a-F/R TGTGAGCCACGACAAATCCA/TGATCTCCCAGCAGCAAACA
PR10b-F/R GAGAGGCTGTGGAAGGTCTG/CCTTTAGCACGTGAGTTGCG
DREB1A-F/R TGGAGCTACTAGAGCTCAATCAACTG/TGGCATCGGAAGCCAGAA
DREB1B-F/R ACAGAGTAGGCAATGAGACTGAGGAT/TTACAGGAATTCATTGACTGCACAT
DREB2A-F/R GGAATCTCCTCCTTTCATCGTG/TTCCGCTCCTGACAAACACG
DREB2B-F/R TTGTGCTTATGACGAGGCAGC/GCTAGTGCAACCTGAACGGAAG
引物名称
Primer name		 引物序列
Primer sequence (5°−3°)
LEA3-F/R CGGCAGCGTCCTCCAAC/CGGTCATCCCCAGCGTG
LIP9-F/R CCTCTTCGACAACCTCCTTGGCA/CTTCCTCATCACTCGACGAGCT
Rab16A-F/R CACACCACAGCAAGAGCTAAGTG/TGGTGCTCCATCCTGCTTAAG
ABI2-F/R TTGTGGAGACTCACGGGCAGTG/CGAGACATTCGTCATCCTTTGC
NCED3-F/R ACGTGATCAAGAAGCCGTACCT/GCTGGTCGAGCGGGATCT
NCED4-F/R GCCGAGACACGCATTGG/GTGAAGGTGGCGACAGCAA
EF1α-F/R TTTCACTCTTGGTGTGAAGCAGAT/GACTTCCTTCACGATTTCATCGTAA

Fig. 1

Relative expression pattern of OsDSK2b gene affected by various stresses and the spatio-temporal expression model of OsDSK2b in Nipponbare A: the relative expression levels of OsDSK2b before and after Guy11, 20% PEG-6000, 150?mmol L-1 NaCl, and 100 μmol L-1ABA treatments. B: the relative expression levels of OsDSK2b in different tissues of Nipponbare (two-week-old seedlings, young roots, node, second leaf, flag leaves, root of booting stage, young panicle, and panicle of heading stage). C: the subcellular localization of OsDSK2b in rice protoplast (Bar: 10 μm). Values are means (± SDs) from three biological replicates (by Dunnett’s test, *: P < 0.05, **: P < 0.01)."

Fig. 2

Knocking out of OsDSK2b enhances rice resistance to blast disease A: the gene structure of OsDSK2b and mutation of target sequence in OsDSK2b knockout strains. Exon and intron are represented by the blank rectangle black line. Red font represents the target sequence in CRISPR vector construction, blue fonts represent the inserted bases, and ellipsis represent the missing bases; B: the phenotype of wild-type Nipponbare and OsDSK2b knockout plants 7 d after inoculation with GD08-T13 using the punch method; C: the lesion sizes of wild-type Nipponbare and OsDSK2b knockout plants 7 d after inoculation with GD08-T13 using the punch method; D: the phenotype of wild-type Nipponbare and OsDSK2b knockout plants 7 d after inoculation with Guy11 in vivo; E: The lesion sizes of wild-type Nipponbare and OsDSK2b knockout plants 7 d after inoculation with Guy11 in vivo. Values are means (± SDs) from three biological replicates (Dunnett’s test, *: P < 0.05, **: P < 0.01)."

Fig. 3

Relative expression levels of pathogenesis-related genes of OsDSK2b The relative expression levels of PR genes in leaves of wild-type Nipponbare and OsDSK2b knockout plants before (0?h) and after (2 d and 4 d) pathogen inoculation with Guy11. Values are means (± SDs) from three biological replicates (Dunnett’s test, *: P < 0.05; **: P < 0.01)."

Fig. 4

Knocking out OsDSK2b increases the tolerance to osmotic stress in rice A: the phenotype of wild-type Nipponbare and OsDSK2b knockout plants under normal condition or 3 d 20% PEG-6000 treatment and 5 d recovery; B: the plant height of wild-type Nipponbare and OsDSK2b knockout plants under normal condition or 3 d 20% PEG-6000 treatment and 5 d recovery; C: the phenotype of wild-type Nipponbare and OsDSK2b knockout plants under normal condition or 5 d 20% PEG-6000 treatment and 5 d recovery; D: the survival rates of wild-type Nipponbare and OsDSK2b knockout plants under normal condition or 5 d 20% PEG-6000 treatment and 5 d recovery; E: the ion leakage of wild-type Nipponbare and OsDSK2b knockout plants before and after osmotic stress treatment; F: the water loss rates of seedlings of wild-type Nipponbare and OsDSK2b knockout plants at 0, 30, 60, 90, 120, 180, 240, and 300?min in vitro. Values are means (± SDs) of three biological replicates (Dunnett’s test, *: P < 0.05; **: P < 0.01)."

Fig. 5

Knocking out OsDSK2b reduces stomatal aperture A: the stomata with different opening degrees. Bar: 10 μm; B: the stomatal proportions of three different degrees of opening on the leaves of wild-type Nipponbare and OsDSK2b knockout plants under normal condition and after 20% PEG-6000 treatment for 4 h. Values are means (± SDs) of three biological replicates, and at least 300 stomata were calculated in each replicate; C: the stomatal density of wild-type Nipponbare and OsDSK2b knockout plants; D: the stomatal size of wild-type Nipponbare and OsDSK2b knockout plants. Values are means (± SDs) of three biological replicates, and at least 100 stomata were calculated in each replicate."

Fig. 6

OsDSK2b regulates the relative expression level of stress-related genes A: the relative expression levels of DREB genes in wild-type Nipponbare and OsDSK2b knockout plants before (0 h) and after (4 h) 20% PEG-6000 treatment; B: the relative expression levels of ABA-related genes in wild-type Nipponbare and OsDSK2b knockout plants before (0 h) and after (4 h) 20% PEG-6000 treatment. Values are means (± SDs) from three biological replicates (Dunnett’s test, *P < 0.05; **P < 0.01)."

Fig. 7

OsDSK2b affects the accumulation of endogenous ABA in rice under 20% PEG-6000 stress treatment Values are means (± SDs) from six biological replicates (Dunnett’s test, *: P < 0.05; **: P < 0.01)."

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