**1. Introduction**

Climate change refers to anomalous atmospheric conditions, as well as sudden unexpected climatic events, such as floods, hurricanes, intense and/or prolonged drought, extreme temperatures, etc. Drought is among the environmental stressors that has the most severe impact on crops throughout the world [1–3]. One-third of arable lands are already defined as arid or semi-arid ones [4], and the severity of drought shows increasing trends [5] since a 5 ◦C increase in mean air temperature is expected in the following years [6–10]. According to experts, the drylands on Earth will increase by 30% and the drier summers and reduced rainfall are expected to affect mostly Asian mid-continental regions, southern Europe, Northern and South Africa [11]. The reduction of usable water sources and the continuous demographic growth make it necessary to improve water use efficiency in the farming sector in order to ensure food security for the years to come. A big step towards this goal has been made by the introduction of soilless cropping systems, where the use of irrigation water is under continuous control [12]. However, the appropriate supply of water to crops, even in soilless conditions, requires the monitoring of various parameters, such as the growth substrate humidity, the climatic and microclimatic conditions, and most importantly, the water status of plants [13], which is more complex to quantify than climatic and growth substrate related parameters [14]. Furthermore, there may be differences between species or even cultivars of the same species in terms of water stress, especially under deficit irrigation conditions where a genotype dependent response is observed. Scientists are looking for mechanisms that regulate the response of plants to water stress, aiming to either identify the most tolerant species or increase tolerance in the sensitive ones. For this

**Citation:** Giordano, M.; Petropoulos, S.A.; Cirillo, C.; Rouphael, Y. Biochemical, Physiological, and Molecular Aspects of Ornamental Plants Adaptation to Deficit Irrigation. *Horticulturae* **2021**, *7*, 107. https://doi.org/10.3390/horticulturae 7050107

Academic Editor: Alessandra Francini

Received: 26 April 2021 Accepted: 6 May 2021 Published: 10 May 2021

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**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

(WUE).

purpose, genetic studies are based on breeding and genetic engineering of model plants, such as *Arabidopsis thaliana* [1,15,16], so that the obtained responses could be extrapolated to other crops such as staple food, medicinal, aromatic, and fiber plants. The efficient use of water is a crucial point in cultivating ornamental plants which have to respond to different needs, e.g., moderate use of natural resources, climate change, environmental pollution, increasing production costs, and maximizing profits [17,18]. Unfortunately, there is still no standard protocol for the irrigation of ornamental species, and water requirements of plants are covered based on growers' personal experience [14,19]. *Horticulturae* **2021**, *7*, x FOR PEER REVIEW 4 of 22

> Knowing the response of different species to water stress conditions would allow the identification of morphological indices and biochemical markers useful for distinguishing sensitive and tolerant species to water deficit stress [20–22]. Therefore, in this review, the morphological, biochemical, physiological, and molecular responses of the main ornamental plants cultivated throughout the world have been studied. Moreover, a literature update regarding the genes involved in ornamental plants' response to water stress is also presented and discussed. Tolerance mechanisms have also been recorded in *Nerium oleander* L., an evergreen shrub belonging to the *Apocynaceae* family which is widespread in dry and semi-arid regions, such as the Mediterranean ones. In the work of Kumar et al. [1], 1-year-old *Oleander* plants were pot grown in a greenhouse and were normally irrigated until acclimatized. Subsequently, they were subjected to water stress and plants were analyzed after 15 and 30 days of stress initiation. The results showed that there were no effects on stem elongation (cm) and fresh weight of leaves (g) after 15 days of stress, whereas the effects became

#### **2. The Effect of Deficit Irrigation on Morphology, Growth, and Quality of Ornamental Plants** Four species belonging to the genus *Sedum* L. (*Crassulaceae* family), namely *Sedum spurium*, *S. ochroleucum*, *S. album*, and *S. sediforme*, also called "Green roofs" and being

significant after 30 days of stress.

The growth and morphology of ornamental plants have an aesthetic value and are very important parameters which guide the consumer's choice. The effects of deficit irrigation on the leaf are related to orientation changes, to reduction of leaf area and leaves number, to reduction of trichomes and canopy area, and to increase in leaf thickness as plant responses to avoid water losses [23–26] (Figure 1, Table 1). used to adorn the urban area and mitigate area pollution, showed different tolerance to water stress implemented with interruption of irrigation for 4 weeks [22]. All species showed a reduction in plant growth, and changes in morphological parameters (stem length, fresh weight) which allowed to establish a gradual tolerance to deficit irrigation.

**Figure 1.** Water stress-induced morphological and physiological changes. (-) reduction due to water stress; (+) increase due to water stress. abscisic acid (ABA); malondialdehyde (MDA); reactive oxygen species (ROS); water use efficiency **Figure 1.** Water stress-induced morphological and physiological changes. (−) reduction due to water stress; (+) increase due to water stress. abscisic acid (ABA); malondialdehyde (MDA); reactive oxygen species (ROS); water use efficiency (WUE).

*Lantana* and *Ligustrum*, two important ornamental plants of the Mediterranean area, showed an increase in spongy and palisade tissue, following severe water stress [24]. The change in the leaf anatomy serves to increased diffusion of CO<sup>2</sup> from the external atmosphere to the spaces between cells [25,27], while thicker leaves presented higher chlorophyll content and photosynthetic activity [27]. Therefore, these responses related to leaf anatomy constitute an avoidance mechanism to reduce water losses.

Water stress has an impact on the morphology of *Chrysanthemum morifolium* Ramat cv. Hj inflorescences, an ornamental plant characterized by ray and disc florets [28]. The

reduction of soil moisture reduces the number and shape of ray florets, while the number of disc florets increases. In *Callistemon citrinus*, the number of inflorescences did not change under moderate stress but reduced when severe stress was implemented [14]. Avoidance mechanisms are also evident in *Viburnum opulus* L. and *Photinia* × *fraseri*, two Mediterranean species which show alterations of leaf parameters under both moderate (60% evapotranspiration [ET]) and severe (30% ET) water stress conditions [27]. The changes in leaf parameters depend on the intensity of water deficit as well as on the genotype.

Reduction in leaf thickness in terms of epidermal thickness, palisade, and spongy tissue, and higher stomatal density have been associated with greater water stress sensitivity in *Passiflora alata* plants [29], whereas *Passiflora setacea* has shown fewer leaf anatomical and is considered more tolerant to deficit irrigation. Moreover, deficit irrigation may change the shape of chloroplasts in *Paeonia ostii* plants, e.g., from an oval shape in control plants to a more rounded shape in stressed plants [30]. All the above-mentioned examples reveal the diversity in plants' responses to water stress related to leaf parameters and highlight the complexity of the defense mechanisms against water stress.

Growth reduction is one of the first manifestations that plants are subjected to with water stress. For example, the application of water stress for one, two, or three weeks decreased the growth of poinsettia (*Euphorbia pulcherrima*) in terms of plant height (67.4, 57.0, and 49.0 cm, respectively) and leaf area (2.91, 1.22, and 0.93 cm<sup>2</sup> , respectively) [18]. In addition, *Rosa damascena* Mill., a rose from Damascus which is widespread all over the world for its perfume and use in cosmetics and medicine, was subjected for 90 days to 100% of field capacity (FC), moderate water stress (50% FC), and severe water stress (25% FC) [10]. On the other hand, the number of leaves was not reduced by stress, so the reduction in aerial biomass was mainly attributed to a reduction in leaf area [31].

*Antirhinum majus* cv. Butterfly is an ornamental plant widely used to beautify urban areas and gardens, which also responds to water stress with a reduction of plant growth parameters (leaves, shoots, flowers), as well as with changes in plant nutritional status (the content of N, P, K, Mg, and Ca) [32]. Similarly, two cultivars of *Matthiola incana* L., an ornamental plant of the *Brassicaceae* family widely appreciated for its beautiful and colorful flowers, was subjected to 5 levels of water stress, namely 90%, 80%, 70%, 60% of field capacity [33].

*Adonis amurensis* and *Adonis pseudoamurensis*, two species belonging to the *Ranunculaceae* family [7] (Table 1), exhibited reduced growth only in the last days of deficit irrigation treatment, indicating that they can tolerate water deficit conditions. Moreover, water stress reduced shoot dry mass in purple coneflower plants (*Echinacea purpurea* L.) by 51.5% [34], while five species of *Passiflora* spp. (*P. edulis*, *P. gibertii*, *P. cincinnata*, *P. alata*, *P. setacea*) showed a reduction in growth within the range of 50–75%, following water deficit conditions [29].

Water stress may also increase the root-to-shoot ratio. This is an adaptive response to deficit irrigation as a result of the increase in the root system growth and the concomitant reduction in the aerial part of the plant [14]. In this way, the plant tries to cope with reduced water availability by increasing water absorption though roots and reducing water loss from leaves at the same time [25,35,36]. Water stress may also cause changes in roots architecture. For example, in *Callistemon citrinus* plants subjected to water stress, the main roots were longer, whereas the growth of small roots, lateral and thinner ones, was eliminated [37]. Similar results were reported for *Nerium oleander* L., *Pittosporum tobira* Thunb., and *Ligustrum japonicum* Thunb. 'Texanum' (Mediterranean ornamental shrubs) plants [12], subjected to four levels of water stress (90%, 80%, 70%, and 60% of container capacity).

Rafi et al. [26] examined the morphological response to water stress in two native, and therefore already adapted to the local climate conditions, ornamental species, namely *Althea rosea* and *Malva sylvestris*, and two exotic ones, namely *Rudbeckia hirta* and *Callistephus chinensis*. The results showed that, concerning roots length, volume, and density, a decreasing trend was observed with increasing water stress severity in the case of *C. chinensis* and *M. sylvestris*. In contrast, in *A. rosea*, the length of the roots increased as

the deficit irrigation levels increased, while roots density decreased in *R. hirta* plants when water stress was more severe.

Three potted Bougainvillea genotypes (*B. glabra* var. Sanderiana, *B.* × *buttiana* 'Rosenka', *B. 'Lindleyana'* (=*B.* '*Aurantiaca*') were grown on three irrigation levels (100%, 50%, and 25% of substrate moisture) and two canopy shapes (globe and pyramid), aiming to identify the most tolerant genotype and the most useful shape [38]. Moreover, the results showed that total dry biomass was reduced as water stress increased, with the *B.* '*Lindleyana*' genotype recording the highest reduction (33%), followed by *B. glabra* var. Sanderiana (20%) and *B.* × *buttiana* 'Rosenka' (5.5%). The effect of water stress on leaves number was the highest in the case of *B.* '*Lindleyana*' plants (reduced by 43%), followed by *B. glabra* var. Sanderiana (reduced by 33%) and *B.* × *buttiana* 'Rosenka' (reduced by 19%). The authors also suggested that the leaf area was reduced (by 43%) by water stress when canopy shape was pyramidal compared to the global one, while water deficit also reduced the content of N, P, and K in the three genotypes examined [38]. Moreover, according to Rouphael et al. [39], water stress is responsible for the reduction in leaf macronutrient contents in plants, probably because of the lower solubilization due to the water deficit, and therefore the lower absorption and translocation of nutrients [40].

Tolerance mechanisms have also been recorded in *Nerium oleander* L., an evergreen shrub belonging to the *Apocynaceae* family which is widespread in dry and semi-arid regions, such as the Mediterranean ones. In the work of Kumar et al. [1], 1-year-old *Oleander* plants were pot grown in a greenhouse and were normally irrigated until acclimatized. Subsequently, they were subjected to water stress and plants were analyzed after 15 and 30 days of stress initiation. The results showed that there were no effects on stem elongation (cm) and fresh weight of leaves (g) after 15 days of stress, whereas the effects became significant after 30 days of stress.

Four species belonging to the genus *Sedum* L. (*Crassulaceae*family), namely *Sedum spurium*, *S. ochroleucum*, *S. album*, and *S. sediforme*, also called "Green roofs" and being used to adorn the urban area and mitigate area pollution, showed different tolerance to water stress implemented with interruption of irrigation for 4 weeks [22]. All species showed a reduction in plant growth, and changes in morphological parameters (stem length, fresh weight) which allowed to establish a gradual tolerance to deficit irrigation.



for a week before treatment begun

Four-month-old seedlings grown in greenhouse, into plastic pots

35–40%, 65–70%, 95–100% of soil water holding capacity (WHC), for 62 days

*Chrysanthemum*

*morifolium* Ramat. cv. Hj Germplasm

K+/Na+

in roots (−)

Ray florets (−)

Disc floret (+) [28]

[1]

[41]


**Table 1.** *Cont.*
