Physiological and morphological features denote that salt stress in Stevia rebaudiana is based on nonstomatic instead of stomatic limitation

Angela Castillejo-Morales; Alfredo Jarma-Orozco; Marcelo F. Pompelli

doi:10.17584/rcch.2021v15i3.12928

Authors

Angela Castillejo-Morales University of Cordoba, Faculty of Agricultural Sciences, Regional Group of Participatory Research of Small Farmers of the Colombian Atlantic Coast INVEPAR, Monteria https://orcid.org/0000-0002-3755-8302
Alfredo Jarma-Orozco University of Cordoba, Faculty of Agricultural Sciences, Regional Group of Participatory Research of Small Farmers of the Colombian Atlantic Coast INVEPAR, Monteria https://orcid.org/0000-0002-5821-2183
Marcelo F. Pompelli Universidade Federal de Pernambuco, Centro de Biociências, Departamento de Botânica, Laboratório de Ecofisiologia Vegetal, Recife https://orcid.org/0000-0002-4408-6374

DOI:

https://doi.org/10.17584/rcch.2021v15i3.12928

Keywords:

Biomass distribution, Disruption between energy input and photosynthesis, Gas exchange, Salinity, Stomatal conductance

Abstract

Stevia rebaudiana is a very widespread plant throughout the world, due to the production of diterpenic steviol glycosides, with high sweetening power, being up to 300 times sweeter than sugar at a concentration of 0.4% (w/v). In the Colombian Caribbean, research has focused on evaluating the adaptation and management of commercial genotypes and experimental lines, however, their behavior against soil salinization is unknown. The objective of this research was to evaluate the response of some physiological and morphological characteristics of two promising genotypes against salt stress. The relationship between gas exchange, chlorophyll a fluorescence, and growth parameters was modulated as a function of the NaCl concentration. Although stomatal conductance and perspiration did not show a response to salt levels, the reduction in net photosynthesis as salinity increased was not associated with stomatal effects, but rather with a drop in the rate of electron transport, which articulates the absorption of light energy and its conversion into photoassimilates. Therefore, it could be inferred that salinity-stressed S. rebaudiana plants are more sensitive to non-stomatal limitation than to stomatal limitation.

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References

Acosta-Motos, J., L. Noguera-Vera, G. Barba-Espín, A. Piqueras, and J. Hernández. 2019. Antioxidant metabolism and chlorophyll fluorescence during the acclimatisation to ex vitro conditions of micropropagated Stevia rebaudiana Bertoni plants. Antioxidants 8(12), 615. Doi: 10.3390/antiox8120615

Basharat, S., Z. Huang, M. Gong, X. Lv, A. Ahmed, I. Hussain, J. Li, G. Du, and L. Liu. 2021. A review on current conventional and biotechnical approaches to enhance biosynthesis of steviol glycosides in Stevia rebaudiana. Chin. J. Chem. Eng. 30, 92-104. Doi: 10.1016/j.cjche.2020.10.018

Batista, K., W. Araújo, W. Antunes, P. Cavatte, G. Moraes, S. Martins, and F. DaMatta. 2012. Photosynthetic limitations in coffee plants are chiefly governed by diffusive factors. Trees 26, 459-468. Doi: 10.1007/s00468-011-0606-2

Brown, M. and A. Forsythe. 1974. Robust tests for equality of variances. J. Am. Stat. Assoc. 69(346), 364-367. Doi: 10.2307/2285659

Cantabella, D., A. Piqueras, J. Acosta-Motos, A. Bernal-Vicente, J. Hernández, and P. Díaz-Vivancos. 2017. Salt-tolerance mechanisms induced in Stevia rebaudiana Bertoni: Effects on mineral nutrition, antioxidative metabolism and steviol glycoside content. Plant Physiol Biochem. 115, 484-496. Doi: 10.1016/j.plaphy.2017.04.023

Centritto, M., F. Loreto, and K. Chartzoulakis. 2003. The use of low [CO2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive saplings. Plant Cell Environ. 26(4), 585-594. Doi: 10.1046/j.1365-3040.2003.00993.x

Cerqueira, J., J. Silveira, F. Carvalho, J. Cunha, and M. Neto. 2019. The regulation of P700 is an important photoprotective mechanism to NaCl‐salinity in Jatropha curcas. Physiol. Plant. 167(3), 404-417. Doi: 10.1111/ppl.12908

Chaves, M.M., J. Flexas, and C. Pinheiro. 2008. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann. Bot. 103(4), 551-560. Doi: 10.1093/aob/mcn125

Debnath, M., N. Ashwath, and D. Midmore. 2019. Physiological and morphological responses to abiotic stresses in two cultivars of Stevia rebaudiana (Bert.) Bertoni. South Afr. J. Bot. 123, 124-132. Doi: 10.1016/j.sajb.2019.01.025

Dos Santos, O., K. Mendes, S. Martins, W. Batista-Silva, M. dos Santos, J. Figueiroa, E. Souza, D. Fernandes, W. Araujo, and M. Pompelli. 2019. Physiological parameters and plasticity as key factors to understand pioneer and late successional species in the Atlantic Rainforest. Acta Physiol. Plant. 41, 145. Doi: 10.1007/s11738-019-2931-9

Flexas, J. and H. Medrano. 2002. Drought‐inhibition of photosynthesis in C3 plants: Stomatal and non‐stomatal limitations revisited. Ann. Bot. 89(2), 183-189. Doi: 10.1093/aob/mcf027

Fonseca-Pereira, P., D. Daloso, J. Gago, A. Nunes-Nesi, and W. Araújo. 2019. On the role of the plant mitochondrial thioredoxin system during abiotic stress. Plant Signal Behav. 14(6), 1592536. Doi: 10.1080/15592324.2019.1592536

González, J., S. Eisa, S. Hussin, and F. Prado. 2015. Quinoa: An incan crop to face Global changes in agriculture. pp. 1-18. In: Murphy, K. and J. Matanguiban (eds.). Quinoa: Improvement and sustainable production. Wiley Blackwell, Hoboken, NJ. Doi: 10.1002/9781118628041.ch1

Hernández-Fernandéz, I., A. Jarma-Orozco, and M. Pompelli. 2021. Allometric models for non-destructive leaf area measurement of stevia: an in depth and complete analysis. Hortic. Bras. 39(2), 205-215. Doi: 10.1590/s0102-0536-20210212

Holbrook, N. 2015. Water balance of plants. pp. 99-118. In: Taiz, L., E. Zeiger, I. Moller, and A. Murphy (eds). Plant physiology and development. 6th ed. Sinauer Associates, Oxford.

Hsie, B., K. Mendes, W. Antunes, L. Endres, M. Campos, F. Souza, N. Santos, B. Singh, E. Arruda, and M. Pompelli. 2015. Jatropha curcas L. (Euphorbiaceae) modulates stomatal traits in response to leaf-to-air vapor pressure deficit. Biomass Bioenerg. 81, 273-281. Doi: 10.1016/j.biombioe.2015.07.014

Huang, L., Z. Li, Q. Liu, G. Pu, Y. Zhang, and J. Li. 2019. Research on the adaptive mechanism of photosynthetic apparatus under salt stress: New directions to increase crop yield in saline soils. Ann. Appl. Biol. 175, 1-17. Doi: 10.1111/aab.12510

Hussin, S., N. Geissler, M. El-Far, and H.-W. Koyro. 2017. Effects of salinity and short-term elevated atmospheric CO2 on the chemical equilibrium between CO2 fixation and photosynthetic electron transport of Stevia rebaudiana Bertoni. Plant Physiol. Biochem. 118, 178-186. Doi: 10.1016/j.plaphy.2017.06.017

Jarma-Orozco, A., E. Combatt-Caballero, and J. Jaraba.-Navas. 2020. Growth and development of Stevia rebaudiana Bert., in high and low levels of radiation. Curr. Plant Biol. 22, 100144. Doi: 10.1016/j.cpb.2020.100144

Mendes, K.R., J.A.A. Granja, J.P. Ometto, A.C.D. Antonio, R.S.C. Menezes, E.C. Pereira, and M.F. Pompelli. 2017. Croton blanchetianus modulates its morphophysiological responses to tolerate drought in a tropical dry forest. Func. Plant Biol. 44(10), 1039-1051. Doi: 10.1071/FP17098

Osmond, B., M. Badger, K. Maxwell, O. Björkman, and R. Leegood. 1997. Too many photons: photorespiration, photoinhibition and photooxidation. Trends Plant Sci. 2(4), 119-121. Doi: 10.1016/S1360-1385(97)80981-8

Pan, T., M. Liu, V. Kreslavski, S. Zharmukhamedov, C. Nie, M. Yu, V. Kuznetsov, S. Allakhverdiev, and S. Shabala. 2021. Non-stomatal limitation of photosynthesis by soil salinity. Crit Rev Environ. Sci. Technol. 51(8), 791-825. Doi: 10.1080/10643389.2020.1735231

Pinho-Pessoa, A.C.B., K.R. Mendes, A. Jarma-Orozco, M.P.S. Pereira, M.A. Santos, R.S.C. Menezes, J.P. Ometto, E.C. Pereira, and M.F. Pompelli. 2018. Interannual variation in temperature and rainfall can modulate the physiological and photoprotective mechanisms of a native semiarid plant species. Indian J. Sci. Technol. 11(41), 1-17. Doi: 10.17485/ijst/2018/v11i42/130972

Pompelli, M., R. Barata-Luís, H. Vitorino, E. Gonçalves, E. Rolim, M. Santos, J. Almeida-Cortez, V. Ferreira, E. Lemos, and L. Endres. 2010. Photosynthesis, photoprotection and antioxidant activity of purging nut under drought deficit and recovery. Biomass Bioenerg. 34(8), 1207-1215. Doi: 10.1016/j.biombioe.2010.03.011

Putnik, P., I. Bezuk, F. Barba, J. Lorenzo, I. Polunić and D. Bursać. 2020. Sugar reduction: Stevia rebaudiana Bertoni as a natural sweetener. pp. 123-152. In: Barba, F., P. Putnik, and D. Kovačević (eds.). Agri-food industry strategies for healthy diets and sustainability. Academic Press, San Diego, CA. Doi: 10.1016/B978-0-12-817226-1.00005-9

Ramesh, K.,V. Singh, and N. Megeji. 2006. Cultivation of stevia [Stevia rebaudiana (Bert.) Bertoni]: a comprehensive review. Adv. Agron. 89, 137-177. Doi: 10.1016/S0065-2113(05)89003-0

Reis, M., L. Coelho, G. Santos, U. Kienle, and J. Beltrão. 2015. Yield response of stevia (Stevia rebaudiana Bertoni) to the salinity of irrigation water. Agr. Water Manage. 152, 217-221. Doi: 10.1016/j.agwat.2015.01.017

Shahverdi, M., H. Omidi, and S. Tabatabaei. 2019. Stevia (Stevia rebaudiana Bertoni) responses to NaCl stress: Growth, photosynthetic pigments, diterpene glycosides and ion content in root and shoot. J. Saudi Soc. Agric. Sci. 18(4), 355-360. Doi: 10.1016/j.jssas.2017.12.001

Shapiro, S. and M. Wilk. 1965. An analysis of variance test for normality (complete samples). Biometrika. 52(3/4), 591-611. Doi: 10.2307/2333709

Silva-Santos, L., N. Corte-Real, J. Dias-Pereira, R. Figueiredo, L. Endres, and M. Pompelli. 2019. Salinity shock in Jatropha curcas leaves is more pronounced during recovery than during stress time. Braz. J. Dev. 5, 11359-11369. Doi: 10.1101/378208

Yu, B., J. Niu, J. Feng, M. Xu, X. Xie, W. Gu, S. Gao, and G. Wang. 2018. Regulation of ferredoxin-NADP+ oxidoreductase to cyclic electron transport in high salinity stressed Pyropia yezoensis. Front. Plant Sci. 9, 1092. Doi: 10.3389/fpls.2018.01092

Zeng, J., A. Chen, D. Li, B. Yi, and W. Wu. 2013. Effects of salt stress on the growth, physiological responses, and glycoside contents of Stevia rebaudiana Bertoni. J. Agric. Food Chem. 61(24), 5720-5726. Doi: 10.1021/jf401237x