This study investigated the effects of recurrent water deficit on drought tolerance traits in black pepper (Piper nigrum L.) 'Bragantina'. Plants were subjected to three cycles of water deficit followed by recovery periods. Water deficit reduced stomatal conductance, photosynthesis, transpiration, and water potential while increasing water-use efficiency. In addition, intercellular CO2 concentration, leaf temperature, root starch, and adaptive morphological characteristics in leaves and roots increased. Despite these adaptations, plants did not recover vegetative growth after rehydration. The primary tolerance mechanisms observed included increased abaxial epidermis thickness, stomatal density, fine roots, periderm thickness, and starch accumulation in roots. Although gas exchange and leaf water potential were restored, vegetative growth did not fully recover. This study highlights the response of black pepper to recurrent water stress and the underlying mechanisms of its drought tolerance.

Capixaba Institute for Research Technical Assistance and Rural Extension BR 101 North Km 151 P O Box 62 Linhares Espírito Santo Brazil

Department of Agrarian and Biological Sciences North Espírito Santo University Center Federal University of Espírito Santo BR 101 North Km 60 Litorâneo District 29932 540 São Mateus Espírito Santo Brazil

Department of Biological Sciences Center for Human and Natural Sciences Federal University of Espírito Santo Avenida Fernando Ferrari 514 Goiabeiras 29075 910 Vitória Espírito Santo Brazil

Federal University of Alfenas Rua Gabriel Monteiro da Silva 700 Center 37048 395 Alfenas Minas Gerais Brazil

Zobrazit více v PubMed

Aires E.S., Ferraz A.K.L., Carvalho B.L. et al.: Foliar application of salicylic acid to mitigate water stress in tomato. – Plants-Basel 11: 1175, 2022. 10.3390/plants11131775 PubMed DOI PMC

Al-Huqail A., El-Dakak R.M., Sanad M.N. et al.: Effects of climate temperature and water stress on plant growth and accumulation of antioxidant compounds in sweet basil (Ocimum basilicum L.) leafy vegetable. – Scientifica 4: 3808909, 2020. 10.1155/2020/3808909 PubMed DOI PMC

Alves R.D.F.B., Menezes-Silva P.E., Sousa L.F. et al.: Evidence of drought memory in Dipteryx alata indicates differential acclimation of plants to savannah conditions. – Sci. Rep.-UK 10: 16455, 2020. 10.1038/s41598-020-73423-3 PubMed DOI PMC

Ambrozim C.S., Furtado J.G., Valani R.S. et al.: [Propagation of black pepper in different concentrations of indolebutyric acid.] – Rev. Ifes Ciênc. 3: 17-28, 2017. [In Portuguese] 10.36524/ric.v3i2.322 DOI

Ambrozim C.S., Medici L.O., Cruz E.S.D. et al.: Physiological response of black pepper (Piper nigrum L.) to deficit irrigation. – Rev. Cienc. Agron. 53: e20207348, 2022. 10.5935/1806-6690.20220002 DOI

Anjorin F.B., Adejumo S.A., Agboola L., Samuel Y.D.: Proline, soluble sugar, leaf starch and relative water contents of four maize varieties in response to different watering regimes. – Cercet. Agron. Mold. XLIX: 51-62, 2016. https://www.researchgate.net/publication/310817911_Proline_Soluble_Sugar_Leaf_Starch_and_Relative_Water_Contents_of_Four_Maize_Varieties_in_Response_to_Different_Watering_Regimes

Barrs H.D., Weatherley P.E.: A re-examination of the relative turgidity technique for estimating water deficit in leaves. – Aust. J. Biol. Sci. 15: 413-428, 1962. 10.1071/BI9620413 DOI

Bertolino L.T., Caine R.S., Gray J.E.: Impact of stomatal density and morphology on water-use efficiency in a changing world. – Front. Plant. Sci. 10: 225, 2019. 10.3389/fpls.2019.00225 PubMed DOI PMC

Blaya-Ros P.J., Blanco V., Torres-Sánchez R., Domingo R.: Drought-adaptive mechanisms of young sweet cherry trees in response to withholding and resuming irrigation cycles. – Agronomy 11: 1812, 2021. 10.3390/agronomy11091812 DOI

Brunetti C., Gori A., Marino G. et al.: Dynamic changes in ABA content in water-stressed Populus nigra: effects on carbon fixation and soluble carbohydrates. – Ann. Bot.-London 124: 627-643, 2019. 10.1093/aob/mcz005 PubMed DOI PMC

Campilho A., Nieminen K., Ragni L.: The development of the periderm: the final boundary between a plant and its environment. – Curr. Opin. Plant Biol. 53: 10-14, 2020. 10.1016/j.pbi.2019.08.008 PubMed DOI

Cerri Neto B., Silva F.R.N., Ferreira T.R. et al.: Responses of wild Piper species to drought and rehydration cycles considering stomatal closure as a marker of the alarm phase. – Photosynthetica 61: 363-376, 2023. 10.32615/ps.2023.030 DOI

Chaves M.M., Flexas J., Pinheiro C.: Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. – Ann. Bot.-London 103: 551-560, 2009. 10.1093/aob/mcn125 PubMed DOI PMC

Conti V., Mareri L., Faleri C. et al.: Drought stress affects the response of Italian local tomato (Solanum lycopersicum L.) varieties in a genotype-dependent manner. – Plants-Basel 8: 336, 2019. 10.3390/plants8090336 PubMed DOI PMC

Cruz E.S.D., Medici L.O., Leles P.S.D.S. et al.: Growth of black pepper plantlets under different substrates and irrigation levels. – Sci. Agric. 79: e20200094, 2022. 10.1590/1678-992X-2020-0094 DOI

Dong S., Beckles D.M.: Dynamic changes in the starch-sugar interconversion within plant source and sink tissues promote a better abiotic stress response. – J. Plant. Physiol. 234-235: 80-93, 2019. 10.1016/j.jplph.2019.01.007 PubMed DOI

Ergo V.V., Lascano R., Vega C.R.C. et al.: Heat and water stressed field-grown soybean: A multivariate study on the relationship between physiological-biochemical traits and yield. – Environ. Exp. Bot. 148: 1-11, 2018. 10.1016/j.envexpbot.2017.12.023 DOI

Fathi A., Tari D.B.: Effect of drought stress and its mechanism in plants. – Int. J. Life Sci. 10: 1-6, 2016. https://www.researchgate.net/publication/294108106_effect_of_drought_stress_and_its_mechanism_in_plants

Ferreira D.F.: Sisvar: a computer statistical analysis system. – Ciênc. Agrotec. 35: 1039-1042, 2011. 10.1590/S1413-70542011000600001 DOI

Galle A., Florez-Sarasa I., El Aououad H., Flexas J.: The Mediterranean evergreen Quercus ilex and the semi-deciduous Cistus albidus differ in their leaf gas exchange regulation and acclimation to repeated drought and re-watering cycles. – J. Exp. Bot. 62: 5207-5216, 2011. 10.1093/jxb/err233 PubMed DOI PMC

George K.J., Malik N., Vijesh Kumar I.P., Krishnamurthy K.S.: Gene expression analysis in drought tolerant and susceptible black pepper (Piper nigrum L.) in response to water deficit stress. – Acta. Physiol. Plant. 39: 104, 2017. 10.1007/s11738-017-2398-5 DOI

Gogosz A.M., Boeger M.R.T., Negrelle R.R.B., Bergo C.: [Comparative leaf anatomy of nine species of the genus Piper (Piperaceae).] – Rodriguésia 63: 405-417, 2012. [In Portuguese] 10.1590/S2175-78602012000200013 DOI

Hamdin N.E., Hussain H., Chong N.F.-M.: Identification of stress-related proteins during the growth and development of Piper nigrum L. – In: IOP Conf. Ser.: Earth Environ. Sci. 549: 012072, 2020. 10.1088/1755-1315/549/1/012072 DOI

He J., Du Y.L., Wang T. et al.: Conserved water use improves the yield performance of soybean (Glycine max (L.) Merr.) under drought. – Agr. Water Manage. 179: 236-245, 2017. 10.1016/j.agwat.2016.07.008 DOI

Johansen D.A.: Plant Microtechnique. Pp. 523. McGraw-Hill Book Company, New York-London: 1940.

Joshi D.R., Shrestha A.C., Adhikari A.: A review on diversified use of the king of spices: Piper nigrum (black pepper). – Int. J. Pharm. Sci. Res. 9: 4089-4101, 2018. https://www.researchgate.net/publication/328215772_A_REVIEW_ON_DIVERSIFIED_USE_OF_THE_KING_OF_SPICES_PIPER_NIGRUM_BLACK_PEPPER

Kraus J.E., Arduin M.: [Basic manual of methods in plant morphology.] Pp. 198. EDUR, Seropédica: 1997. [In Portuguese]

Krishnamurthy K.S., Ankegowda S.J., Umadevi P., George J.K.: Black pepper and water stress. – In: Rao N., Shivashankara K., Laxman R. (ed.): Abiotic Stress Physiology of Horticultural Crops. Pp. 321-332. Springer, New Delhi: 2016. 10.1007/978-81-322-2725-0_17 DOI

Li P., Yang H., Wang L. et al.: Physiological and transcriptome analyses reveal short-term responses and formation of memory under drought stress in rice. – Front. Genet. 10: 55, 2019. 10.3389/fgene.2019.00055 PubMed DOI PMC

MacRae J.C., Armstrong D.G.: Enzymatic method for determination of α-linked glucose polymers in biological materials. – J. Sci. Food Agr. 19: 578-581, 1968. 10.1002/jsfa.2740191006 DOI

Mantoan L.P.B., Corrêa C.V., Rainho C.A., de Almeida L.F.R.: Rapid dehydration induces long-term water deficit memory in sorghum seedlings: advantages and consequences. – Environ. Exp. Bot. 180: 104252, 2020. 10.1016/j.envexpbot.2020.104252 DOI

Marcos F.C.C., Silveira N.M., Mokochinski J.B. et al.: Drought tolerance of sugarcane is improved by previous exposure to water deficit. – J. Plant. Physiol. 223: 9-18, 2018. 10.1016/j.jplph.2018.02.001 PubMed DOI

Menezes-Silva P.E., Sanglard L.M.V.P., Ávila R.T. et al.: Photosynthetic and metabolic acclimation to repeated drought events play key roles in drought tolerance in coffee. – J. Exp. Bot. 68: 4309-4322, 2017. 10.1093/jxb/erx211 PubMed DOI

Mickky B.M., Abbas M.A., El-Shhaby O.A.: Alterations in photosynthetic capacity and morpho-histological features of leaf in alfalfa plants subjected to water deficit-stress in different soil types. – Indian J. Plant. Physiol. 23: 426-443, 2018. 10.1007/s40502-018-0383-7 DOI

Miller G.L.: Use of dinitrosalicylic acid reagent for determination of reducing sugar. – Anal. Chem. 31: 426-428, 1959. 10.1021/ac60147a030 DOI

Monda K., Mabuchi A., Negi J., Iba K.: Cuticle permeability is an important parameter for the trade-off strategy between drought tolerance and CO2 uptake in land plants. – Plant Signal. Behav. 16: 1908692, 2021. 10.1080/15592324.2021.1908692 PubMed DOI PMC

Nascimento M.E.., Potiguara R.C.V.: [Anatomical aspects of the vegetative organs of Piper hispidinervium C.DC. (Piperaceae) and their secretory structures.] – Boletim do Museu Paraense Emílio Goeldi 15: 39-104, 1999. [In Portuguese] https://repositorio.museu-goeldi.br/handle/mgoeldi/619

Negi A., Kokkat J.G., Jasrotia R.S. et al.: Drought responsiveness in black pepper (Piper nigrum L.): Genes associated and development of a web-genomic resource. – Physiol. Plantarum 172: 669-683, 2021. 10.1111/ppl.13308 PubMed DOI

Pompelli M.F., Espitia-Romero C.A., Jaraba-Navas J.D. et al.: Stevia rebaudiana under a CO2 enrichment atmosphere: Can CO2 enrichment overcome stomatic, mesophilic and biochemical barriers that limit photosynthesis? – Sustainability 14: 14269, 2022. 10.3390/su142114269 DOI

Prezotti L.C., Gomes J.A., Dadalto G.G., Oliveira J.A.: [Liming and fertilization recommendation manual for the State of Espírito Santo.] Pp. 289. SEEA, INCAPER, CEDAGRO Vitória; 2007. [In Portuguese] https://biblioteca.incaper.es.gov.br/digital/handle/123456789/3242

Rivas R., Falcão H.M., Ribeiro R.V. et al.: Drought tolerance in cowpea species is driven by less sensitivity of leaf gas exchange to water deficit and rapid recovery of photosynthesis after rehydration. – S. Afr. J. Bot. 103: 101-107, 2016. 10.1016/j.sajb.2015.08.008 DOI

Rizzini C.T.: [Treatise of Phytogeography of Brazil.] Pp. 374. Editora de Humanismo, Ciência e Tecnologia, São Paulo: 1976. [In Portuguese] 10.1590/S1983-40632013000200012 DOI

Salehi-Lisar S.Y., Bakhshayeshan-Agdam H.: Drought stress in plants: causes, consequences, and tolerance. – In: Hossain M., Wani S., Bhattacharjee S. et al. (ed.): Drought Stress Tolerance in Plants. Vol. 1. Pp. 1-16. Springer, Cham: 2016. 10.1007/978-3-319-28899-4_1 DOI

Schmildt E.R., Arantes L.O., Hell L.H. et al.: [Black pepper varieties.] – In: Silva M.B., Da Vitória E.L., Campanharo A. (ed.): [Black Pepper Culture.] Pp. 19-39. Araçá, São Mateus: 2018. [In Portuguese] 10.1590/S1983-40632013000200012 DOI

Scholasch T., Rienth M.: Review of water deficit mediated changes in vine and berry physiology; Consequences for the optimization of irrigation strategies. – OENO One 53: 423-444, 2019. 10.20870/oeno-one.2019.53.3.2407 DOI

Segatto F.B., Bisognin D.A., Benedetti M. et al.: [A technique for the anatomical study of potato leaf epidermis.] – Ciênc. Rural 34: 1597-1601, 2004. [In Portuguese] https://www.redalyc.org/pdf/331/33134542.pdf

Shukla P.S., Shotton K., Norman E. et al.: Seaweed extract improve drought tolerance of soybean by regulating stress-response genes. – AoB Plants 10: plx051, 2018. 10.1093/aobpla/plx051 PubMed DOI PMC

Silva T.I., Dias M.G., Grossi J.A.S. et al.: Application of phytohormones as attenuators of salt stress in Tropaeolum majus L. (Tropaeolaceae). – Acta. Bot. Croat. 81: 51-60, 2022. 10.37427/botcro-2022-001 DOI

Souza P.U., Lima L.K.S., Soares T.L. et al.: Biometric, physiological and anatomical responses of Passiflora spp. to controlled water deficit. – Sci. Hortic.-Amsterdam 229: 77-90, 2018. 10.1016/j.scienta.2017.10.019 DOI

Strock C.F., Lynch J.P.: Secondary root growth: an unexplored component of soil resource acquisition. – Ann. Bot.-London 126: 205-218, 2020. 10.1093/aob/mcaa068 PubMed DOI PMC

Sulok K.M.T.A., Haruna A.O., Shang C.Y. et al.: Leaf stomatal density and distribution in black pepper under field conditions. – J. Trop. Plant Physiol. 11: 24-31, 2019. https://www.mspp.org.my/files/jtpp/jttpvol11/JTPPVol11(1)2019page24-31Pipernigrum.pdf

Takooree H., Aumeeruddy M.Z., Rengasamy K.R.R. et al.: A systematic review on black pepper (Piper nigrum L.): from folk uses to pharmacological applications. – Crit. Rev. Food Sci. Nutr. 59: S210-S243, 2019. 10.1080/10408398.2019.1565489 PubMed DOI

Tardieu F., Draye X., Javaux M.: Root water uptake and ideotypes of the root system: whole-plant controls matter. – Vadose Zone J. 16: 1-10, 2017. 10.2136/vzj2017.05.0107 DOI

Thivend P., Mercier C., Guilbot A.: Dosage de l'amidon dans les milieux complexes. – Ann. Biol. Anim. Bioch. Biophys. 5: 513-526, 1965. [In French] 10.1051/rnd:19650407 DOI

Tombesi S., Frioni T., Poni S., Palliotti A.: Effect of water stress “memory” on plant behavior during subsequent drought stress. – Environ. Exp. Bot. 150: 106-114, 2018. 10.1016/J.ENVEXPBOT.2018.03.009 DOI

Wasaya A., Zhang X., Fang Q., Yan Z.: Root phenotyping for drought tolerance: a review. – Agronomy 8: 241, 2018. 10.3390/agronomy8110241 DOI

Witkowski E.T.F., Lamont B.B.: Leaf specific mass confounds leaf density and thickness. – Oecologia 88: 486-493, 1991. 10.1007/BF00317710 PubMed DOI

Yan W., Zhong Y., Shangguan Z.: Rapid response of the carbon balance strategy in Robinia pseudoacacia and Amorpha fruticosa to recurrent drought. – Environ. Exp. Bot. 138: 46-56, 2017. 10.1016/j.envexpbot.2017.03.009 DOI

Yemm E.W., Willis A.J.: The estimation of carbohydrates in plant extracts by anthrone. – Biochem. J. 57: 508-514, 1954. 10.1042/bj0570508 PubMed DOI PMC

Zanandrea I., Alves J.D., Deuner S. et al.: Tolerance of Sesbania virgata plants to flooding. – Aust. J. Bot. 57: 661-669, 2010. 10.1071/BT09144 DOI

Zhao W., Sun Y., Kjelgren R., Liu X.: Response of stomatal density and bound gas exchange in leaves of maize to soil water deficit. – Acta Physiol. Plant. 37: 1704, 2015. 10.1007/s11738-014-1704-8 DOI

Zulfiqar F., Younis A., Riaz A et al.: Morpho-anatomical adaptations of two Tagetes erecta L. cultivars with contrasting response to drought stress. – Pak. J. Bot. 52: 801-810, 2020. 10.30848/PJB2020-3(35) DOI