Research progress of peptides discovery and function in resistance to abiotic stress in plant

Abstract

Plant peptides play crucial roles in various biological processes, including stress responses. This study investigates the functions of plant peptides in response to different adversity stresses, focusing on drought, salt, high temperature, and other environmental challenges. In drought conditions, specific peptides such as CLE25 and CLE9 were found to regulate stomatal closure and root architecture to enhance the efficiency of water utilization. Salt stress induces the expression of CAPE1 and CEP3, which are involved in ion homeostasis and osmoregulation, thereby contributing to salt tolerance in plants. Heat stress triggers the expression of peptides such as CEL45, which contributes to the heat tolerance of cells. Besides, we have also verified a new class of non-conventional peptides, and a large number of non-conventional peptides have been identified in rice seedlings. Understanding the origin and functions of these peptides presents both challenges and opportunities for developing stress-resistant crops. Future research should focus on elucidating the precise molecular mechanisms of peptide-mediated stress responses and exploring their potential applications in agriculture and biotechnology.

Keywords

Biological Sciences / Plant Biology / Agricultural and Veterinary Sciences / Crop and Pasture Production

References

[1] AggarwalS, KumarA, JainM, SudanJ, SinghK, KumariS, MustafizA. C-terminally encoded peptides (CEPs) are potential mediators of abiotic stress response in plants. Physiol Mol Biol Plants, 2020, 26102019-33.

[2] AhangerMA, AgarwalRM. Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L) as influenced by potassium supplementation. Plant Physiol Biochem, 2017, 115: 449-60.

[3] Ali U, Tian L, Tang R, Wang S, Luo W, Liu S, Zhang J, Wu L (2024) A comprehensive atlas of endogenous peptides in maize. iMeta 3(6):e247. https://doi.org/10.1002/imt2.247

[4] AndrewsSJ, RothnagelJA. Emerging evidence for functional peptides encoded by short open reading frames. Nat Rev Genet, 2014, 153193-204.

[5] BashyalS, GautamCK, MüllerLM. CLAVATA signaling in plant-environment interactions. Plant Physiol, 2024, 19431336-57.

[6] Betsuyaku S, Sawa S, Yamada M (2011) The Function of the CLE Peptides in Plant Development and Plant-Microbe Interactions. Arabidopsis Book 9:e0149. https://doi.org/10.1199/tab.0149

[7] BiA, WangT, WangG, ZhangL, WassieM, AmeeM, XuH, HuZ, LiuA, FuJ, ChenL, HuT. Corrigendum for: Stress memory gene FaHSP17.8-CII controls thermotolerance via remodeling PSII and ROS signaling in tall fescue. Plant Physiol, 2022, 1881670.

[8] BirnbaumKD, Sánchez AlvaradoA. Slicing across kingdoms: regeneration in plants and animals. Cell, 2008, 1324697-710.

[9] ButenkoMA, SimonR. Beyond the meristems: similarities in the CLAVATA3 and INFLORESCENCE DEFICIENT IN ABSCISSION peptide mediated signalling pathways. J Exp Bot, 2015, 66175195-203.

[10] ChenJ, BrunnerAD, CoganJZ, NuñezJK, FieldsAP, AdamsonB, ItzhakDN, LiJY, MannM, LeonettiMD, WeissmanJS. Pervasive functional translation of noncanonical human open reading frames. Science (New York), 2020, 36764821140-6.

[11] ChienPS, NamHG, ChenYR. A salt-regulated peptide derived from the CAP superfamily protein negatively regulates salt-stress tolerance in Arabidopsis. J Exp Bot, 2015, 66175301-13.

[12] ChuH, QianQ, LiangW, YinC, TanH, YaoX, YuanZ, YangJ, HuangH, LuoD, MaH, ZhangD. The floral organ number4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice. Plant Physiol, 2006, 14231039-52.

[13] CousoJP, PatraquimP. Classification and function of small open reading frames. Nat Rev Mol Cell Biol, 2017, 189575-89.

[14] CzyzewiczN, ShiCL, VuLD, Van De CotteB, HodgmanC, ButenkoMA, De SmetI. Modulation of Arabidopsis and monocot root architecture by CLAVATA3/EMBRYO SURROUNDING REGION 26 peptide. J Exp Bot, 2015, 66175229-43.

[15] DelayC, IminN, DjordjevicMA. CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants. J Exp Bot, 2013, 64175383-94.

[16] EndoA, SawadaY, TakahashiH, OkamotoM, IkegamiK, KoiwaiH, SeoM, ToyomasuT, MitsuhashiW, ShinozakiK, NakazonoM, KamiyaY, KoshibaT, NambaraE. Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol, 2008, 14741984-93.

[17] EndoS, ShinoharaH, MatsubayashiY, FukudaH. A novel pollen-pistil interaction conferring high-temperature tolerance during reproduction via CLE45 signaling. Current Biology, 2013, 23171670-6.

[18] GautratP, LaffontC, FrugierF, RuffelS. Nitrogen Systemic Signaling: From Symbiotic Nodulation to Root Acquisition. Trends Plant Sci, 2021, 264392-406.

[19] Haag AF, Kerscher B, Dall’Angelo S, Sani M, Longhi R, Baloban M, Wilson HM, Mergaert P, Zanda M, Ferguson GP (2012) Role of cysteine residues and disulfide bonds in the activity of a legume root nodulespecific, cysteine-rich peptide. J Biol Chem 287(14):10791–10798. https://doi.org/10.1074/jbc.M111.311316

[20] HarutaM, SabatG, SteckerK, MinkoffBB, SussmanMR. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science (New York), 2014, 3436169408-11.

[21] HirakawaY, SawaS. Diverse function of plant peptide hormones in local signaling and development. Curr Opin Plant Biol, 2019, 51: 81-7.

[22] IuchiS, KobayashiM, TajiT, NaramotoM, SekiM, KatoT, TabataS, KakubariY, Yamaguchi-ShinozakiK, ShinozakiK. Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J, 2001, 274325-33.

[23] JacksonR, KroehlingL, KhitunA, BailisW, JarretA, YorkAG, KhanOM, BrewerJR, SkadowMH, DuizerC, HarmanCCD, ChangL, BieleckiP, SolisAG, SteachHR, SlavoffS, FlavellRA. The translation of non-canonical open reading frames controls mucosal immunity. Nature, 2018, 5647736434-8.

[24] Jun J, Fiume E, Roeder AH, Meng L, Sharma VK, Osmont KS, Baker C, Ha CM, Meyerowitz EM, Feldman LJ, Fletcher JC (2010) Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol 154(4):1721–1736. https://doi.org/10.1104/pp.110.163683

[25] KamranM, ParveenA, AhmarS, MalikZ, HussainS, ChatthaMS, SaleemMH, AdilM, HeidariP, ChenJT. An Overview of Hazardous Impacts of Soil Salinity in Crops, Tolerance Mechanisms, and Amelioration through Selenium Supplementation. Int J Mol Sci, 2019, 211148.

[26] KumarK, KumarM, KimSR, RyuH, ChoYG. Insights into genomics of salt stress response in rice. Rice (New York), 2013, 6127

[27] LayKS, TakahashiH. Nutrient-Responsive Small Signaling Peptides and Their Influence on the Root System Architecture. Int J Mol Sci, 2018, 19123927.

[28] LiX, HanH, ChenM, YangW, LiuL, LiN, DingX, ChuZ. Overexpression of OsDT11, which encodes a novel cysteine-rich peptide, enhances drought tolerance and increases ABA concentration in rice. Plant Mol Biol, 2017, 931–221-34.

[29] LiB, GaoK, RenH, TangW. Molecular mechanisms governing plant responses to high temperatures. J Integr Plant Biol, 2018, 609757-79.

[30] Luo W, Xiao Y, Liang Q, Su Y, Xiao L (2019) Identification of Potential Auxin-Responsive Small Signaling Peptides through a Peptidomics Approach in Arabidopsis thaliana. Molecules 24(17):3146. https://doi.org/10.3390/molecules24173146

[31] MaJ, WardCC, JungreisI, SlavoffSA, SchwaidAG, NeveuJ, BudnikBA, KellisM, SaghatelianA. Discovery of human sORF-encoded polypeptides (SEPs) in cell lines and tissue. J Proteome Res, 2014, 1331757-65.

[32] MaW, ZhangC, ZhangW, ShengP, XuM, NiY, ChenM, ChengB, ZhangX. TMT-Based Comparative Peptidomics Analysis of Rice Seedlings under Salt Stress: An Accessible Method to Explore Plant Stress-Tolerance Processing. J Proteome Res, 2022, 21122905-19.

[33] MarshallE, CostaLM, Gutierrez-MarcosJ. Cysteine-rich peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development. J Exp Bot, 2011, 6251677-86.

[34] MathewMM, PrasadK. Model systems for regeneration: Arabidopsis. Development (Cambridge, England), 2021, 1486dev19534.

[35] MatsubayashiY. Small post-translationally modified Peptide signals in Arabidopsis. The Arabidopsis Book, 2011, 9: e0150.

[36] MitchumMG, WangX, DavisEL. Diverse and conserved roles of CLE peptides. Curr Opin Plant Biol, 2008, 11175-81.

[37] MotteH, VannesteS, BeeckmanT. Molecular and Environmental Regulation of Root Development. Annu Rev Plant Biol, 2019, 70: 465-88.

[38] MurphyE, SmithS, De SmetI. Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell, 2012, 2483198-217.

[39] NakaminamiK, OkamotoM, Higuchi-TakeuchiM, YoshizumiT, YamaguchiY, FukaoY, ShimizuM, OhashiC, TanakaM, MatsuiM, ShinozakiK, SekiM, HanadaK. AtPep3 is a hormone-like peptide that plays a role in the salinity stress tolerance of plants. Proc Natl Acad Sci USA, 2018, 115225810-5.

[40] Ogawa-OhnishiM, YamashitaT, KakitaM, NakayamaT, OhkuboY, HayashiY, YamashitaY, NomuraT, NodaS, ShinoharaH, MatsubayashiY. Peptide ligand-mediated trade-off between plant growth and stress response. Science (New York), 2022, 3786616175-80.

[41] ParkinMC, WeiH, O'CallaghanJP, KennedyRT. Sample-dependent effects on the neuropeptidome detected in rat brain tissue preparations by capillary liquid chromatography with tandem mass spectrometry. Anal Chem, 2005, 77196331-8.

[42] PearceG, StrydomD, JohnsonS, RyanCA. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science (New York), 1991, 2535022895-7.

[43] PillitteriLJ, PetersonKM, HorstRJ, et al. . Molecular profiling of stomatal meristemoids reveals new component of asymmetric cell division and commonalities among stem cell populations in Arabidopsis. Plant Cell, 2011, 2393260-75.

[44] PlazaS, MenschaertG, PayreF. In Search of Lost Small Peptides. Annu Rev Cell Dev Biol, 2017, 33: 391-416.

[45] RenJ, FengL, GuoL, GouH, LuS, MaoJ. Genome-wide identification and expression analysis of the BURP domain-containing genes in Malus domestica. Physiol Mol Biol Plants, 2023, 29111717-31.

[46] RobertsI, SmithS, StesE, De RybelB, StaesA, van de CotteB, NjoMF, DedeyneL, DemolH, LavenusJ, AudenaertD, GevaertK, BeeckmanT, De SmetI. CEP5 and XIP1/CEPR1 regulate lateral root initiation in Arabidopsis. J Exp Bot, 2016, 67164889-99.

[47] SakataT, OshinoT, MiuraS, TomabechiM, TsunagaY, HigashitaniN, MiyazawaY, TakahashiH, WatanabeM, HigashitaniA. Auxins reverse plant male sterility caused by high temperatures. Proc Natl Acad Sci USA, 2010, 107198569-74.

[48] SecherA, KelstrupCD, Conde-FrieboesKW, PykeC, RaunK, WulffBS, OlsenJV. Analytic framework for peptidomics applied to large-scale neuropeptide identification. Nat Commun, 2016, 7: 11436.

[49] SmithS, ZhuS, JoosL, RobertsI, NikonorovaN, VuLD, StesE, ChoH, LarrieuA, XuanW, GoodallB, van de CotteB, WaiteJM, RigalA, Ramans HarboroughS, PersiauG, VannesteS, KirschnerGK, VandermarliereE, MartensL, De SmetI. The CEP5 Peptide Promotes Abiotic Stress Tolerance, As Revealed by Quantitative Proteomics, and Attenuates the AUX/IAA Equilibrium in Arabidopsis. Mol Cell Proteomics, 2020, 1981248-62.

[50] SongXF, HouXL, LiuCM. CLE peptides: critical regulators for stem cell maintenance in plants. Planta, 2021, 25515.

[51] SparksE, WachsmanG, BenfeyPN. Spatiotemporal signalling in plant development. Nat Rev Genet, 2013, 149631-44.

[52] SugimotoK, TemmanH, KadokuraS, MatsunagaS. To regenerate or not to regenerate: factors that drive plant regeneration. Curr Opin Plant Biol, 2019, 47: 138-50.

[53] TabataR, SawaS. Maturation processes and structures of small secreted peptides in plants. Front Plant Sci, 2014, 5: 311.

[54] TakahashiF, SuzukiT, OsakabeY, BetsuyakuS, KondoY, DohmaeN, FukudaH, Yamaguchi-ShinozakiK, ShinozakiK. A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature, 2018, 5567700235-8.

[55] TakahashiF, HanadaK, KondoT, ShinozakiK. Hormone-like peptides and small coding genes in plant stress signaling and development. Curr Opin Plant Biol, 2019, 51: 88-95.

[56] TavorminaP, De ConinckB, NikonorovaN, De SmetI, CammueBP. The Plant Peptidome: An Expanding Repertoire of Structural Features and Biological Functions. Plant Cell, 2015, 2782095-118.

[57] TostAS, KristensenA, OlsenLI, AxelsenKB, FuglsangAT. The PSY Peptide Family-Expression, Modification and Physiological Implications. Genes, 2021, 122218.

[58] VriensK, CammueBP, ThevissenK. Antifungal plant defensins: mechanisms of action and production. Molecules (Basel, Switzerland), 2014, 19812280-303.

[59] WangG, ZhangG, WuM. CLE Peptide Signaling and Crosstalk with Phytohormones and Environmental Stimuli. Front Plant Sci, 2016, 6: 1211.

[60] WangP, WangY, RenF. Genome-wide identification of the CLAVATA3/EMBRYO SURROUNDING REGION (CLE) family in grape (Vitis vinifera L.). BMC Genomics, 2019, 201553.

[61] WangS, TianL, LiuH, LiX, ZhangJ, ChenX, JiaX, ZhengX, WuS, ChenY, YanJ, WuL. Large-Scale Discovery of Non-conventional Peptides in Maize and Arabidopsis through an Integrated Peptidogenomic Pipeline. Mol Plant, 2020, 1371078-93.

[62] WuH. Plant salt tolerance and Na+ sensing and transport. Crop J, 2018, 6: 215-25.

[63] YangW, ZhaiH, WuF, DengL, ChaoY, MengX, ChenQ, LiuC, BieX, SunC, YuY, ZhangX, ZhangX, ChangZ, XueM, ZhaoY, MengX, LiB, ZhangX, ZhangD, LiC. Peptide REF1 is a local wound signal promoting plant regeneration. Cell, 2024, 187123024-3038.e14.

[64] YuY, LiW, LiuY, LiuY, ZhangQ, OuyangY, DingW, XueY, ZouY, YanJ, JiaA, YanJ, HaoX, GouY, ZhaiZ, LiuL, ZhengY, ZhangB, XuJ, YangN, YanJ. A Zea genus-specific micropeptide controls kernel dehydration in maize. Cell, 2024, S0092–86742401212-1

[65] Zhang L, Shi X, Zhang Y, Wang J, Yang J, Ishida T, Jiang W, Han X, Kang J, Wang X et al (2019) CLE9 peptide-induced stomatal closure is mediated by abscisic acid, hydrogen peroxide, and nitric oxide in Arabidopsis thaliana. Plant Cell Environ 42(3):1033–1044. https://doi.org/10.1111/pce.13475

[66] ZhangZ, LiuL, KucukogluM, TianD, LarkinRM, ShiX, ZhengB. Predicting and clustering plant CLE genes with a new method developed specifically for short amino acid sequences. BMC Genomics, 2020, 211709.

[67] ZhangZ, LiuC, LiK, LiX, XuM, GuoY. CLE14 functions as a "brake signal" to suppress age-dependent and stress-induced leaf senescence by promoting JUB1-mediated ROS scavenging in Arabidopsis. Mol Plant, 2022, 151179-88.

[68] ZhouH, XiaoF, ZhengY, LiuG, ZhuangY, WangZ, ZhangY, HeJ, FuC, LinH. PAMP-INDUCED SECRETED PEPTIDE 3 modulates salt tolerance through RECEPTOR-LIKE KINASE 7 in plants. Plant Cell, 2022, 342927-44.

[69] ZhuX, RenX, XiongL, LiuT, BaiX. Genetic dissection of crayfish (Procambarus clarkii) high temperature tolerance and assessment of the potential application in breeding of the HSP genes. Comp Biochem Physiol Part D Genomics Proteomics, 2024, 52: 101330. Advance online publication

[70] ZulfiqarF, AkramNA, AshrafM. Osmoprotection in plants under abiotic stresses: new insights into a classical phenomenon. Planta, 2019, 25113.

Funding

Natural Science Foundation of Hubei Province(202310701201614)

RIGHTS & PERMISSIONS

The Author(s)