Interactions between ShPP2-1, an F-box family gene, and ACR11A regulate cold tolerance of tomato

Jianwen Song , Lele Shang , Shiwei Chen , Yongen Lu , Yuyang Zhang , Bo Ouyang , Zhibiao Ye , Junhong Zhang

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 148

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :148 DOI: 10.1038/s41438-021-00582-3
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Interactions between ShPP2-1, an F-box family gene, and ACR11A regulate cold tolerance of tomato
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Abstract

There is a critical need to identify germplasm resources and genes that promote cold tolerance of tomato because global tomato production is threatened by cold stress. We found that the expression of an F-box gene family member named ShPP2-1 from Solanum habrochaites is cold inducible and studied its contribution to cold tolerance. Overexpression of ShPP2-1 in cultivated tomato (AC) reduced cold tolerance by intensifying damage to cell membranes. To explore the underlying molecular mechanism, we conducted a yeast two-hybrid library screen and found that a protein containing ACT domain repeats named ACR11A interacts with PP2-1. Overexpression of SlACR11A in AC enhanced the cold tolerance of seedlings and germinating seeds. Cold tolerance decreased in tomato plants that overexpressed both of these genes. Additionally, we performed seed germination experiments in the cold with 177 tomato accessions and identified two alleles of SlACR11A that differ in one single-nucleotide polymorphism. We found that one of these alleles, SlACR11AG, is significantly enriched in cold-tolerant tomato plants. Taken together, our findings indicate that the combination of low expression levels of PP2-1 and high expression levels of ACR11A can promote cold tolerance. These genes may therefore serve as direct targets for both genetic engineering and improvement projects that aim to enhance the cold tolerance of tomato.

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Jianwen Song, Lele Shang, Shiwei Chen, Yongen Lu, Yuyang Zhang, Bo Ouyang, Zhibiao Ye, Junhong Zhang. Interactions between ShPP2-1, an F-box family gene, and ACR11A regulate cold tolerance of tomato. Horticulture Research, 2021, 8 (1) : 148 DOI:10.1038/s41438-021-00582-3

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References

[1]

Raza, A. et al. Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants 8, 34 (2019).

[2]

Shi, Y., Ding, Y. & Yang, S. Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci. 23, 623-637 (2018).

[3]

Ding, Y., Shi, Y. & Yang, S. Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. N. Phytol. 222, 1690-1704 (2019).

[4]

Ding, Y., Shi, Y. & Yang, S. Molecular regulation of plant responses to environmental temperatures. Mol. Plant 13, 544-564 (2020).

[5]

Zhang, X. et al. Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J. 39, 905-919 (2004).

[6]

Ye, C. et al. Cold tolerance in rice varieties at different growth stages. Crop Pasture Sci. 60, 328-338 (2009).

[7]

Ma, Y. et al. COLD1 confers chilling tolerance in rice. Cell 160, 1209-1221 (2015).

[8]

Wang, F. et al. Phytochrome A and B function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling. Plant Physiol. 170, 459-471 (2016).

[9]

Wang, F. et al. Crosstalk of PIF4 and DELLA modulates CBF transcript and hormone homeostasis in cold response in tomato. Plant Biotechnol. J. 18, 1041-1055 (2020).

[10]

Zhuang, K. et al. Whirly1 enhances tolerance to chilling stress in tomato via protection of photosystem II and regulation of starch degradation. N. Phytol. 221, 1998-2012 (2019).

[11]

Foolad, M. R., Subbiah, P. & Zhang, L. Common QTL affect the rate of tomato seed germination under different stress and nonstress conditions. Int. J. Plant Genom. 2007, 97386 (2007).

[12]

Foolad, M. R., Chen, F. Q. & Lin, G. Y. RFLP mapping of QTLs conferring cold tolerance during seed germination in an interspecific cross of tomato. Mol. Breed. 4, 519-529 (1998).

[13]

Foolad, M. R., Lin, G. Y. & Chen, F. Q. Comparison of QTLs for seed germination under non-stress, cold stress and salt stress in tomato. Plant Breed. 118, 167-173 (1999).

[14]

KAZMI, R. H. et al. Complex genetics controls natural variation among seed quality phenotypes in a recombinant inbred population of an interspecific cross between Solanum lycopersicum×Solanum pimpinellifolium. Plant Cell Environ. 35, 929-951 (2012).

[15]

Abd-Hamid, N.-A., Ahmad-Fauzi, M.-I., Zainal, Z. & Ismail, I. Diverse and dynamic roles of F-box proteins in plant biology. Planta 251, 68 (2020).

[16]

Kipreos, E. T. & Pagano, M. The F-box protein family. Genome Biol. 1, reviews3002.1 (2000).

[17]

Dinant, S. et al. Diversity of the superfamily of phloem lectins (Phloem Protein 2) in angiosperms. Plant Physiol. 131, 114-128 (2003).

[18]

Li, Y. et al. The SCF E3 ligase AtPP2-B11 plays a negative role in response to drought stress in Arabidopsis. Plant Mol. Biol. Rep. 32, 943-956 (2014).

[19]

Cheng, C. et al. SCFAtPP2-B11 modulates ABA signaling by facilitating SnRK2.3 degradation in Arabidopsis thaliana. PLoS Genet. 13, e1006947 (2017).

[20]

Jia, F. et al. SCF E3 ligase PP2-B11 plays a positive role in response to salt stress in Arabidopsis. J. Exp. Bot. 66, 4683-4697 (2015).

[21]

Aravind, L. & Koonin, E. V. Gleaning non-trivial structural, functional and evolutionary information about proteins by iterative database searches. J. Mol. Biol. 287, 1023-1040 (1999).

[22]

Liberles, J., Thórólfsson, M. & Martinez, A. Allosteric mechanisms in ACT domain containing enzymes involved in amino acid metabolism. Amino Acids 28, 1-12 (2005).

[23]

Hsieh, M.-H. & Goodman, H. M. Molecular characterization of a novel gene family encoding ACT domain repeat proteins in Arabidopsis. Plant Physiol. 130, 1797-1806 (2002).

[24]

Sung, T.-Y., Chung, T.-Y., Hsu, C.-P. & Hsieh, M.-H. The ACR11 encodes a novel type of chloroplastic ACT domain repeat protein that is coordinately expressed with GLN2 in Arabidopsis. BMC Plant Biol. 11, 118 (2011).

[25]

Singh, S. K. et al. ACR11 modulates levels of reactive oxygen species and salicylic acid-associated defense response in Arabidopsis. Sci. Rep. 8, 11851 (2018).

[26]

Liu, H. et al. Differential modulation of photosynthesis, signaling, and transcriptional regulation between tolerant and sensitive tomato genotypes under cold stress. PLoS One 7, e50785 (2012).

[27]

Campos, P. S., Quartin, V. N., Ramalho, J. C. & Nunes, M. A. Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J. Plant Physiol. 160, 283-292 (2003).

[28]

Liu, H. et al. Overexpression of ShDHN, a dehydrin gene from Solanum habrochaites enhances tolerance to multiple abiotic stresses in tomato. Plant Sci. 231, 198-211 (2015).

[29]

Yu, C. et al. ShCIGT, a Trihelix family gene, mediates cold and drought tolerance by interacting with SnRK1 in tomato. Plant Sci. 270, 140-149 (2018).

[30]

Jenkins, J. A. The origin of the cultivated tomato. Economic Bot. 2, 379-392 (1948).

[31]

Lin, T. et al. Genomic analyses provide insights into the history of tomato breeding. Nat. Genet. 46, 1220-1226, http://www.nature.com/ng/journal/v46/n11/abs/ng.3117.html#supplementary-information (2014).

[32]

Paran, I. & van der Knaap, E. Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. J. Exp. Bot. 58, 3841-3852 (2007).

[33]

Zhu, G. et al. Rewiring of the fruit metabolome in tomato breeding. Cell 172, 249-261.e12 (2018).

[34]

Soyk, S. et al. Bypassing negative epistasis on yield in tomato imposed by a domestication gene. Cell 169, 1142-1155 e12 (2017).

[35]

Li, R. et al. FIS1 encodes a GA2-oxidase that regulates fruit firmness in tomato. Nat. Commun. 11, 5844 (2020).

[36]

Wang, Z. et al. Loss of salt tolerance during tomato domestication conferred by variation in a Na(+)/K(+) transporter. EMBO J. https://doi.org/10.15252/embj.2019103256 (2020).

[37]

Song, J. et al. MAPK11 regulates seed germination and ABA signaling in tomato by phosphorylating SnRKs. J. Exp. Bot. 72, 1677-1690 (2021).

[38]

Song, J. et al. An ATL78-like RING-H2 finger protein confers abiotic stress tolerance through interacting with RAV2 and CSN5B in tomato. Front. Plant Sci. 7, 1305 (2016).

[39]

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408 (2001).

[40]

Ouyang, B. et al. Transformation of tomatoes with osmotin and chitinase genes and their resistance to Fusarium wilt. J. Hortic. Sci. Biotech. 80, 517-522 (2005). ://WOS:000232378000003.

[41]

Yoo, S.-D., Cho, Y.-H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572 (2007).

[42]

Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874 (2016).

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