SlCV affects starch metabolism by regulating SlBAM3 stability under low night temperature stress in tomatoes

Jiazhi Lu , Yu Chen , Tianyi Zhang , Feng Wan , Mingfang Qi , Tianlai Li , Yufeng Liu

Horticulture Research ›› 2025, Vol. 12 ›› Issue (12) : 233

PDF (2629KB)
Horticulture Research ›› 2025, Vol. 12 ›› Issue (12) :233 DOI: 10.1093/hr/uhaf233
Article
research-article
SlCV affects starch metabolism by regulating SlBAM3 stability under low night temperature stress in tomatoes
Author information +
History +
PDF (2629KB)

Abstract

Nocturnal starch remobilization is critical for plant carbon allocation and stress adaptation. While β-amylase 3 (BAM3) serves as the primary catalyst for starch degradation at night, its regulation mechanisms under stress remain to be fully characterized. The chloroplast vesiculation (CV) protein is crucial for maintaining chloroplast homeostasis during stress conditions, though its potential involvement in starch metabolic processes remains unexplored. Herein, we show that low night temperature (LNT) stress induces starch accumulation in tomato leaves, with SlCV overexpression exacerbating this phenotype and compromising LNT tolerance, whereas SlCV silencing promotes starch catabolism. RNA-seq and metabolome analyses detected lower levels of starch metabolites and amylase activity in SlCV overexpression plants. Strikingly, we have confirmed the physical interaction between SlCV and SlBAM3, and SlCV overexpression significantly accelerated the degradation of SlBAM3 under LNT stress, while SlCV knockout enhanced the stability of SlBAM3. Genetic validation confirmed that SlBAM3-silenced plants accumulate excessive starch and exhibit LNT-sensitive phenotypes, and SlBAM3 overexpression enhances cold tolerance. Furthermore, SlBAM3 complementation rescues the starch overaccumulation and LNT hypersensitivity of SlCV overexpression plants. These results elucidate the regulatory mechanism of starch metabolism mediated by SlCV and associated with SlBAM3 protein stability, providing novel insights into the starch metabolic pathway under cold stress.

Cite this article

Download citation ▾
Jiazhi Lu, Yu Chen, Tianyi Zhang, Feng Wan, Mingfang Qi, Tianlai Li, Yufeng Liu. SlCV affects starch metabolism by regulating SlBAM3 stability under low night temperature stress in tomatoes. Horticulture Research, 2025, 12(12): 233 DOI:10.1093/hr/uhaf233

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgments

This study was supported by the National Natural Science Foundation of China (Grant Nos. 32072651, 31772356, 32272791), the earmarked fund for CARS (CARS-23), Liaoning Revitalization Talents Program (Grant No. XLYC2203065), Liaoning Province Outstanding Youth Fund project (Grant No. 2024JH3/50100026), and Shenyang Agricultural University high-level personnel training (Grant No. 2023Y003).

Author contributions

Y.L. and J.L. conceived and designed the experiments; J.L., Y.C., and T.Z. participated in experiments and data analyses; J.L. and Y.C. wrote the manuscript with inputs and guidance from F.W., M.F., T.L., and Y.L. All authors have read and approved the final manuscript.

Data availability

The authors confirm that data from this study are available.

Conflict of interest statement

The authors declare no conflicts of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Lee K, Kang H. Recent insights into the physio-biochemical and molecular mechanisms of low temperature stress in tomato. Plants. 2024; 13:2715

[2]

Apriyanto A, Compart J, Fettke J. A review of starch, a unique biopolymer-structure, metabolism and in planta modifications. Plant Sci. 2022; 318:111223

[3]

Ribeiro C, Stitt M, Hotta CT. How stress affects your bud-get—stress impacts on starch metabolism. Front Plant Sci. 2022; 13:774060

[4]

Du S, Cai Y, Qiu S. et al. Metabolic profiling of Oryza sativa L.triggered by chilling stress using ultraperformance liquid chromatography coupled with quadrupole/time-of-flight mass spectrometry (UPLC-QTOF-MS) with transcriptome analysis. J Agric Food Chem. 2022; 70:15703-14

[5]

Jiang J, Hou R, Yang N. et al. Physiological and TMT-labeled proteomic analyses reveal important roles of sugar and sec-ondary metabolism in citrus junos under cold stress. JProteome. 2021; 237:104145

[6]

Li M, Yue T, Han J. et al. Exogenous glucose irrigation alleviates cold stress by regulating soluble sugars, ABA and photosynthesis in melon seedlings. Plant Physiol Biochem. 2024; 217:109214

[7]

Liu YF, Qi MF, Li TL. Photosynthesis, photoinhibition, and antiox-idant system in tomato leaves stressed by low night temperature and their subsequent recovery. Plant Sci. 2012; 196:8-17

[8]

Liu YF, Zhang GX, Qi MF. et al. Effects of calcium on photo-synthesis, antioxidant system, and chloroplast ultrastructure in tomato leaves under low night temperature stress. J Plant Growth Regul. 2015; 34:263-73

[9]

Smith AM, Zeeman SC. Starch: a flexible, adaptable carbon store coupled to plant growth. Annu Rev Plant Biol. 2020; 71:217-45

[10]

Liang G, Hou Y, Wang H. et al. VaBAM1 weakens cold tolerance by interacting with the negative regulator VaSR1 to suppress β-amylase expression. Int J Biol Macromol. 2023; 225:1394-404

[11]

Monroe JD, Storm AR. The Arabidopsis β-amylase (BAM) gene family: diversity of form and function. Plant Sci. 2018; 276:163-70

[12]

Fulton DC, Stettler M, Mettler T. et al. β-AMYLASE4, a noncat-alytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell. 2008; 20:1040-58

[13]

Soyk S, šimková K, Zürcher E. et al. The enzyme-like domain of Arabidopsis nuclear β-amylases is critical for DNA sequence recognition and transcriptional activation. Plant Cell. 2014; 26: 1746-63

[14]

Monroe JD, Storm AR, Badley EM. et al. β-Amylase1 and β-amylase3 are plastidic starch hydrolases in Arabidopsis that seem to be adapted for different thermal, pH, and stress con-ditions. Plant Physiol. 2014; 166:1748-63

[15]

Horrer D, Flütsch S, Pazmino D. et al. Blue light induces a distinct starch degradation pathway in guard cells for stomatal opening. Curr Biol. 2016; 26:362-70

[16]

Storm AR, Kohler MR, Berndsen CE. et al. Glutathionyla-tion inhibits the catalytic activity of Arabidopsis β-amylase3 but not that of paralog β-amylase1. Biochemistry. 2018; 57: 711-21

[17]

Wang S, Blumwald E. Stress-induced chloroplast degradation in Arabidopsis is regulated via a process independent of autophagy and senescence-associated vacuoles. Plant Cell. 2014; 26: 4875-88

[18]

Lu J, Yu J, Liu P. et al. Ubiquitin-mediated degradation of SlPsbS regulates low night temperature tolerance in tomatoes. Cell Rep. 2024; 43:114757

[19]

Pan T, Liu Y, Hu X. et al. Stress-induced endocytosis from chloroplast inner envelope membrane is mediated by CHLORO-PLAST VESICULATION but inhibited by GAPC. Cell Rep. 2023; 42: 113208

[20]

Sade N, Umnajkitikorn K, Rubio Wilhelmi MD. et al. Delaying chloroplast turnover increases water-deficit stress tolerance through the enhancement of nitrogen assimilation in rice. JExp Bot. 2018; 69:867-78

[21]

Kamranfar I, Xue GP, Tohge T. et al. Transcription factor RD26 is a key regulator of metabolic reprogramming during dark-induced senescence. New Phytol. 2018; 218:1543-57

[22]

Ahouvi Y, Haber Z, Zach YY. et al. The alteration of tomato chloroplast vesiculation positively affects whole-plant source-sink relations and fruit metabolism under stress conditions. Plant Cell Physiol. 2022; 63:2008-26

[23]

Barros JA, Cavalcanti JH, Pimentel KG. et al. The interplay between autophagy and chloroplast vesiculation pathways under dark-induced senescence. Plant Cell Environ. 2023; 46: 3721-36

[24]

Botticella E, Testone G, Buffagni V. et al. Mutations in starch biosynthesis genes affect chloroplast development in wheat pericarp. Plant Physiol Biochem. 2024; 207:108354

[25]

Yu JC, Lu JZ, Cui XY. et al. Melatonin mediates reactive oxygen species homeostasis via SlCV to regulate leaf senescence in tomato plants. J Pineal Res. 2022; 73:e12810

[26]

Zhu H, Yang X, Wang X. et al. The sweetpotato β-amylase gene IbBAM1.1 enhances drought and salt stress resistance by regulating ROS homeostasis and osmotic balance. Plant Physiol Biochem. 2021; 168:167-76

[27]

Zhang Y, Zhu J, Khan M. et al. Transcription factors ABF4 and ABR1 synergistically regulate amylase-mediated starch catabolism in drought tolerance. Plant Physiol. 2023b; 191: 591-609

[28]

Mutava RN, Prince SJ, Syed NH. et al. Understanding abiotic stress tolerance mechanisms in soybean: a comparative evaluation of soybean response to drought and flooding stress. Plant Physiol Biochem. 2015; 86:109-20

[29]

Zhou H, Li Q, Gichuki DK. et al. Dynamics of starch degrada-tion and expression of related genes during chilling stress in grapevine. Hortic Adv. 2023; 1:3

[30]

Umnajkitikorn K, Sade N, Rubio Wilhelmi MD. et al. Silencing of OsCV (chloroplast vesiculation) maintained photorespiration and N assimilation in rice plants grown under elevated CO2. Plant Cell Environ. 2020; 43:920-33

[31]

Stettler M, Eicke S, Mettler T. et al. Blocking the metabolism of starch breakdown products in Arabidopsis leaves triggers chloro-plast degradation. Mol Plant. 2009; 2:1233-46

[32]

Martin C, Smith AM. Starch biosynthesis. Plant Cell. 1995; 7:971

[33]

Edner C, Li J, Albrecht T. et al. Glucan, water dikinase activ-ity stimulates breakdown of starch granules by plastidial β-amylases. Plant Physiol. 2007; 145:17-28

[34]

Monroe JD. Involvement of five catalytically active Arabidopsis β-amylases in leaf starch metabolism and plant growth. Plant Direct. 2020; 4:e00199

[35]

Sharma KD, Patil G, Kiran A. Characterization and differential expression of sucrose and starch metabolism genes in contrast-ing chickpea (Cicer arietinum L.) genotypes under low tempera-ture. J Genet. 2021; 100:71

[36]

Zhang Y, Peng Y, Liu J. et al. Tetratricopeptide repeat protein SlREC2 positively regulates cold tolerance in tomato. Plant Phys-iol. 2023a; 192:648-65

[37]

Liu Q, Li X, Fettke J. Starch granules in Arabidopsis thaliana mesophyll and guard cells show similar morphology but differences in size and number. Int J Mol Sci. 2021; 22: 5666

[38]

Lu J, Yin Z, Lu T. et al. Cyclic electron flow modulates the linear electron flow and reactive oxygen species in tomato leaves under high temperature. Plant Sci. 2020; 292:110387

[39]

Dong X, Duan S, Wang HB. et al. Plastid ribosomal protein LPE2 is involved in photosynthesis and the response to C/N balance in Arabidopsis thaliana. J Integr Plant Biol. 2020; 62:1418-32

[40]

Wang F, Yan J, Ahammed GJ. et al. PGR5/PGRL1 and NDH mediate far-red light-induced photoprotection in response to chilling stress in tomato. Front Plant Sci. 2020; 11:669

[41]

Turner MF, Heuberger AL, Kirkwood JS. et al. Non-targeted metabolomics in diverse sorghum breeding lines indicates pri-mary and secondary metabolite profiles are associated with plant biomass accumulation and photosynthesis. Front Plant Sci. 2016; 7:953

PDF (2629KB)

419

Accesses

0

Citation

Detail

Sections
Recommended

/