Introduction

Drought and salinity are conditions in some soils that limit agricultural production worldwide, due to the fact that they produce a series of morphological, physiological and biochemical effects that negatively affect the growth and development of crops (^{Munns and Tester, 2008}). Worldwide, drought and salinity influence at least 75 countries (^{Qadir et al., 1997}).

In the case of Mexico, the levels of effects due to salinity cover around one million ha (Serrato et al., 2002), so it is expected that productivity and crop yields will be affected in more 50% for the second half of this century (^{Reyes et al., 2014}).

To combat the effects of salinity and rehabilitate the soils that have been affected, various studies have proposed the implementation of phytodesalination; this is a sustainable agricultural practice, which consists of the use of various halophyte species that have the ability to extract significant amounts of sodium (Na⁺) from the affected environment and remove it through the absorption of plant roots and its translocation to the stems and leaves (^{Nouri et al., 2017}).

The relevance of this practice lies in the ability of these species to desalinate saline soils in a relatively inexpensive way, present a low level of disturbance in the soils where it is implemented and provide additional income to farmers at the end of their cultivation, since they can be used as fodder, biofuels, medicines and food for man (^{Nikalje et al., 2018}).

However, since phytodesalination is a practice that demands a large amount of plant material per hectare (^{McSorley et al., 2016}), by having to take plants from their habitat to transfer them to the sites that are intended to be remedied, the implementation of this practice can lead to an intensive exploitation of the species, to the point of putting its gene pool at risk in the absence of protocols that ensure its production in a sustainable way.

Hence the need to find new alternatives that allow the massive propagation of plant material, at low cost for farmers, in the shortest possible time; this must be done, without losing sight of the homogeneity in the quality of the plants, the supply flow and the continuous availability in the agricultural field.

According to ^{Veras et al. (2018)}, an effective alternative to solve the shortage of seeds and plant material is vegetative or asexual propagation, which is based on the principle of totipotency (^{Cabahug et al., 2018}), which means that each cell of plants contains the genetic information necessary to form new individuals with characteristics identical to those of the mother plant.

This can be done through cuttings from the stem, since in addition to shortening the propagation period, making its management efficient and reducing production costs, it allows to maintain the genetic characteristics of the parent plant and transmit it from generation to generation (^{Ramos-Hernández et al., 2013}). Above all, it can be an optimal strategy for late-rooting species (^{Tosta et al., 2012}).

The asexual vegetative propagation through cuttings, generally relies on growth regulators in order to stimulate the rooting of the cuttings for their correct development, due to their influence on cell division and elongation. Such is the case of indole butyric acid (IBA), a synthetic auxin that has proven to be effective in stimulating cell production and growth, as well as intervening in different activities of the plant, such as: stem growth, root formation, the inhibition of lateral buds, abscission of leaves and fruits, as well as the activation of cambium cells (^{Akwatulira et al., 2011}).

Figure 1 Images of the basal-intermediate and intermediate-apical portions (a); and from the S. verrucosum cuttings (b) 90 days after the application of the IBA. 

According to several studies, IBA is possibly the best growth regulator for general use, because it is not toxic to plants in a wide range of concentration levels, it has greater stability against degradation and metabolism and is usually even more effective than other growth regulators such as indoleacetic acid IAA (^{Ludwig-Müller, 2000}).

Although it is true that asexual vegetative propagation has been implemented in numerous species of great commercial relevance, such as: Annona diversifolia Saff. (Annonaceae) (Orozco-Castillo and González-Esquinca, 2017), Punica granatum L. (Lythraceae) (^{Singh, 2014}), Stevia rebaudiana Bertoni (Asteraceae) (^{López-Medina et al., 2016}), Vanilla planifolia (Orchidaceae) (^{Azofeifa-Bolaños et al., 2018}), so far there are no operative rooting protocols that effectively guide the production of succulent halophyte species.

This may be due to the fact that the optimal IBA concentration varies according to the species and the endogenous level of phytohormones that are present in the mother plants during the cuttings (^{Cabahug et al., 2018}). Recently, it was reported that, in the municipality of Villamar, Michoacán, Mexico, a perennial native halophyte species with enormous phytodesalination potential grows called Sesuvium verrucosum by bioaccumulating 0.96 t ha^-1 of Na⁺ (^{Lastiri-Hernández et al., 2020}), a dicotyledonous of the Aizoaceae family with C₃ photosynthesis, which has a wide phenotypic plasticity due to the formation of successive changes that this species has developed in its ontogenetic system, such as secondary thickening patterns and the formation of the internal phloem, which they allow for greater mechanical resistance, flexibility and above all, a greater storage capacity for water and cations, mainly Na⁺ (^{Elbar, 2015}).

However, in the absence of research and an operating protocol that helps to establish the bases for the correct development of the halophyte S. verrucosum; through cuttings, the objective of this work was to determine the rooting capacity and analyze the magnitude changes in its biometric parameters, from different concentrations in the hormonal treatment.

Materials and methods

The study was carried out under greenhouse conditions during the period of July-September 2019, which is located in the municipality of Jiquilpan de Juárez, Michoacán, Mexico, at an altitude of 1 560 meters above sea level and coordinates 19° 59’ 57.6456” North latitude and -102° 42’ 24.0336” West longitude. On average, the temperature and relative humidity conditions in the greenhouse were 36/10 °C (day/night) and 60% (±10%), respectively.

Results and discussion

Table 1 shows the effects of auxin IBA on the roots of S. verrucosum cuttings, after being exposed to different concentrations during a period of 90 days. The treatments evaluated, both in the basal-intermediate and intermediate-apical portions of the S. verrucosum cuttings, showed significant differences (p≤ 0.05) in all the variables evaluated with respect to their own control, mainly when the cuttings were subjected to high IBA concentrations. At 2 000 and 4 000 mg L^-1 IBA concentration, no difference could be observed.

These results suggest that, at concentrations higher than those established in the present study, phytotoxic effects could be triggered in S. verrucosum cuttings, which would lead to a reduction in the quality of the adventitious root system (^{Delgado et al., 2008}). In addition, it was found that the intermediate-apical portion achieved higher rooting percentages than the basal-intermediate portion, varying in 25%, 8.33%, 8.33%, 8.33%, 16.67% and 8.33% among the treatments evaluated at 0, 800, 1 200, 1 600, 2 000 and 4 000 mg L^-1 of IBA, respectively (Table 1). Hence, the rooting capacity of S. verrucosum cuttings drastically decreases in the basipetal direction.

Similarly, it was found that the intermediate-apical portion achieved a higher phytomass than the basal-intermediate portion, achieving increases of 29.69% and 20.22% in the fresh and dry weight of the root, in the treatments used as control, 30.13 % and 21.07% between the treatments evaluated at 800 mg L^-1, 33.95% and 24.77% between the treatments evaluated at 1200 mg L^-1, 36.79% and 27.13% between the treatments evaluated at 1 600 mg L^-1, 39.08% and 30.02% among the treatments evaluated at 2 000 mg L^-1 and 38.17% and 29.15% among the treatments evaluated at 4 000 mg L^-1 of IBA, respectively (Table 1).

Regarding the length of the roots, it was found that the intermediate-apical portion achieved greater increases, compared to the basal-intermediate portion, by varying in 8.5%, 8.84%, 9.69%, 10.14%, 12.54% and 11.08% among treatments evaluated at 0, 800, 1 200, 1 600, 2 000, and 4 000 mg L^-1 of IBA, respectively.

On the other hand, it was observed that the intermediate-apical portion achieved a greater increase in the number of roots, compared to the basal-intermediate portion, by varying in 26.88%, 22.80%, 16.76%, 13.54%, 8.41% and 6.99 % among treatments evaluated at 0, 800, 1 200, 1 600, 2 000, and 4 000 mg L^-1 of IBA, respectively. However, at 4 000 mg L^-1 of IBA, no significant differences (p≤ 0.05) were observed between these two portions.

The fact that the cuttings of the intermediate-apical portion showed a greater increase in the percentage of rooting, fresh and dry weight of the root, as well as in the number of roots with respect to the basal-intermediate portion, could be explained by the high concentrations of endogenous auxins that accumulate in this portion of the stem (^{Mustafa and Khan, 2016}), which facilitate the biosynthesis pathways and a wide variety of development processes, among which are: the beginning of leaf primordia, phototropism, cell division and differentiation of vascular tissues, which as a whole, promote the production of adventitious roots (^{Vanneste and Friml, 2009}). This translates into a better absorption of the root system, to the benefit of the vigor obtained in the aerial part of the cuttings (^{López-Acosta et al., 2008}), a situation that was reflected through the number, length and production of root phytomass as IBA concentration levels increased.

In addition to this, the higher percentage of rooting, formation and size of the root system in the cuttings of the intermediate-apical portion, can be attributed to various factors, among which are: a) the photosynthesis process in the leaves, as the main organ carbohydrate synthesizer for the plant; b) the formation of young leaves, as a source of photoassimilates, responsible for the production of auxins and cofactors that are essential in the process of cell division; c) the polar transport of auxins, responsible for the auxins being synthesized in the apical meristem and translocated towards the basal part of the plants; d) the porosity of the substrate and the depth of the transplantation of the cuttings, both responsible for the penetration of the roots, the mobilization and translocation of nutrients. As well as an adequate water balance within the cuttings; and e) the physicochemical conditions of the substrate to guarantee adequate aeration and moisture retention conditions (^{Akwatulira et al., 2011}; ^{López-Medina et al., 2016}; ^{Ferriani et al., 2018}).

Table 2 shows the effects of auxin IBA on the aerial part of S. verrucosum cuttings, after being exposed to different concentrations during a period of 90 days. The treatments evaluated, both in the basal-intermediate and intermediate-apical portions of the S. verrucosum cuttings, showed significant differences (p≤ 0.05) in all the variables evaluated with respect to their own control, mainly when the cuttings were subjected to high IBA concentrations.

The aerial part of the cuttings from both the basal-intermediate and intermediate-apical portions did not show significant differences in the concentration levels of 2 000 and 4 000 mg L^-1 of IBA. Regarding the fresh and dry weight of the aerial part, it was found that the intermediate-apical portion was greater than the basal-intermediate portion, achieving increases of 30.24% and 22.05%, respectively, among the treatments used as control, 31.38% and 23.52% between the treatments evaluated at 800 mg L^-1, 34.06% and 26.34% between the treatments evaluated at 1 200 mg L^-1, 37.01% and 28.61% between the treatments evaluated at 1 600 mg L^-1, 40.04% and 32.79% between the treatments evaluated at 2 000 mg L^-1 and 39.78% and 30.86% between the treatments evaluated at 4 000 mg L^-1 of IBA.

Regarding the diameter of the stem, it was found that the intermediate-apical portion achieved greater increases, compared to the basal-intermediate portion, by varying in 2.14%, 2.78%, 3.91%, 4.30%, 4.77% and 4.41% between treatments. evaluated at 0, 800, 1 200, 1 600, 2 000, and 4 000 mg L^-1 IBA, respectively.

Regarding the total height of the cuttings, it was observed that the intermediate-apical portion was greater than the basal-intermediate portion, achieving increases of 4.58%, 5.37%, 6.18%, 6.49%, 6.88% and 6.58%. among treatments evaluated at 0, 800, 1 200, 1 600, 2 000, and 4 000 mg L^-1 of IBA, respectively. Unlike the concentration level of 4 000 mg L^-1, where no significant difference (p≤ 0.05) was observed between both portions (Table 2).

According to ^{Vercruyssen et al. (2011)}, the architecture of the roots provides an important anchor for plants and allows the synthesis of hormones that influence the development of sprouts, these factors could have led to the intermediate-apical portion achieving a greater increase in the phytomass of the aerial part, as well as better energy activity.

In addition, the effectiveness in the percentage of rooting from the concentration of 800 mg L^-1 of IBA, both in the basal-intermediate and intermediate-apical portions of the S. verrucosum cuttings, confirmed the low requirement of exogenous auxins that they are needed to trigger their rooting; this shows that the species is easy to root. This could be explained by the processes that take place during rooting, such as: the accumulation of metabolites at the site of application of auxins, the synthesis of new proteins and the division of the vascular cells of the cambium (^{Mehta et al., 2018}). According to ^{Veras et al. (2018)}, from the exogenous application of IBA, the formation of tracheids is stimulated by differentiation of callus cells, mainly in the xylem, which in turn leads to a greater production and formation of adventitious roots.

However, from the concentration of 2 000 mg L^-1 of IBA in both the basal-intermediate and intermediate-apical portions of the S. verrucosum cuttings, no significant differences were observed (p≤ 0.05) in terms of the increase in the variables studied (biomass of the root and aerial part, length of the root, number of roots, diameter of the stem and height of the plants), which may be due to the rooting speed and the sprouts that were originated in response to the IBA concentration, since the optimal dose depends on each species (^{Carranza et al., 2012}).

To this, it must be added that several studies have indicated that the existence of endophytic bacteria, present in the species S. verrucosum, promote the growth of these plants and their physiology, by altering their regulation processes in osmotic pressure, changes in the responses of the stomata, the adjustment in the morphology of the root size, the modification of nitrogen accumulation and metabolism, the production of hormones such as auxins, gibberellins and zeatin, as well as the absorption and translocation of certain minerals (^{El-Awady et al., 2015}).

Conclusions

The results of this research showed that the use of IBA to treat cuttings of the species S. verrucosum, improved the rooting rate and the magnitude of the biometric parameters, both in the intermediate-apical portion and in the basal-intermediate portion.

Also, it was found that with the use of clay soil and manure in a ratio (5:1), the massive spread of S. verrucosum benefits; by presenting a high growth and survival rate that is potentiated with the help of IBA, mainly to 2 000 mg L^-1.

Therefore, through this method of propagation, it can contribute to safeguarding the most vulnerable sectors, especially in regions with low productive systems, given the high salinity conditions in which they are immersed.