Physiological and biochemical characterization of six Prunus rootstocks in response to flooding
Introduction
Peaches [Prunus persica (L.) Batsch.] and nectarines (Prunus persica var. nucipersica) are major stone fruit crops with worldwide production occupying 1,712,425 ha and yields of 142,800 kg ha−1 in 2018 (FAOSTAT, 2018). These crops are mostly grown in warm temperate regions such as the Mediterranean with limited water supply, high irradiance, and high summer temperatures (Jimenez et al., 2013). During the past 40 years, subtropical breeding programs have developed Prunus cultivars suited to subtropical environments (i.e. Florida in the U.S.) that require fewer hours (< 200) of chilling to induce flowering compared to traditional cultivars that require 500–1500 chilling temperatures to induce flowering (George and Erez, 2000). However, in these subtropical areas, stone fruit is vulnerable to root hypoxia due to flooding from heavy rains during tropical storms and hurricanes. Additionally, as a result of increased incidences of heavy rainfall due to climate change, subtropical areas including Florida, have experienced increased crop loss due to flooding (Bailey-Serres et al., 2012; EPA, 2016).
Plant flooding stress is caused by depletion of soil oxygen, which often results in serious repercussions to crop growth and development (Schaffer et al., 1992). Once the soil becomes hypoxic (Ashraf, 2012), the pH will move towards a neutral state and the redox potential will be altered. This can lead to changes in soil nutrient element concentrations and the release of phytotoxic compounds, such as H2S, that will exacerbate crop stress (Laanbrock, 1990; Gries et al., 1990). In numerous fruit crop species, including stone fruit, stomatal conductance (gs) is adversely affected by flooding, leading to a reduction in net CO2 assimilation (A) (Schaffer et al., 1992). The reduction in A is likely linked to low CO2 levels as a result of changes in stomatal aperture (Pezeshki, 2001). A decline in intercellular CO2 concentration results in adverse effects on the electron transport chain leading to the creation of reactive oxygen species (ROS) (Mahajan and Tuteja, 2005) such as hydroxyl radical (OH−), superoxide radical (O2−), and hydrogen peroxide (H2O2), which are commonly upregulated as a stress response (Shahid et al., 2019). Increased ROS activity can also reduce chlorophyll content, leading to further reductions in A (Pimentel et al., 2014). ROS can damage nucleic acids, lipids, and proteins via oxidation, which could be mitigated by the antioxidant defense system. This defense system is composed of enzymatic antioxidants such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), ascorbate peroxidase (APX), guaiacol peroxidase (GPX), monodehydroascorbate reductase (MDHAR), and glutathione reductase (GRT) along with non-enzymatic low-molecular antioxidant metabolites such as ascorbate acid (AsA) and Glutathione (GSH) (Gill and Tuteja, 2010). Antioxidants and antioxidant metabolites scavenge ROS by converting them into water and oxygen, making them non-toxic to the plant. The balance between antioxidant activity and ROS formation indicates the level of oxidative damage that will occur (Gill and Tuteja, 2010). Since flooding stress leads to an increase in ROS formation, antioxidant levels could serve as an indicator of flooding tolerance.
Osmolytes alleviate oxidative damage caused by ROS and protects protein from ROS-induced disintegration (Sharma and Dubey, 2005). Organic solutes including proline, glycinebetaine, total soluble sugars, and total free amino acids have also been found to protect the cell wall structure of various proteins, and thus play role in resilience to abiotic stressors (Mattoo et al., 2015). Proline is an essential amino acid regulating primary metabolism during growth and development (Barickman et al., 2019). Proline also protects cellular structures from degradation due to oxidative damage (Liang et al., 2013). Glycinebetaine is another important osmolyte, thought to have positive effects on enzyme and membrane integrity. Glycinebetaine has been linked to improved tolerance against several abiotic stresses (Shahid et al., 2019). Though the aforementioned metabolic activities can drastically reduce plant growth, they can be exacerbated by the uptake of toxic heavy metals including iron and manganese. The changes in soil redox potential associated with low soil O2 can lead to an abundance of toxic heavy metals, which have been found to reduce root and shoot growth, alter transport systems, breakdown chlorophyll, and reduce gs, resulting in a steep decline in A (Andersen, 1991; Schaffer et al., 1992).
Early physiological responses to root hypoxia are often not visible. However, if roots are subjected to hypoxia for a sufficient time, visible responses such as wilting, chlorosis, necrosis, marginal browning of the leaves, defoliation, epinasty, and fruit drop will become apparent (Schaffer et al., 1992). A rootstock that allows Prunus spp. to tolerate conditions of short-term root hypoxia and thus survive and recover from flooding is needed for subtropical production areas where low-chill stone fruit are grown. Among Prunus rootstocks, those with genetic background from plum (Prunus subg. prunus) have been considered to have resistance to flooding stress, whereas those crossed with almond (Prunus dulcis) are highly susceptible (Zieglar et al., 2017). We compared peach, plum, and plum x peach rootstocks, all grafted with the peach scion UFSun, a low-chill cultivar adapted for subtropical climates (Sarkhosh, 2018). The objective was to investigate the physiological response of six Prunus rootstocks grafted with cv. UFsun to flooding of the root zone. Leaf gas exchange (A and gs), ROS, enzymatic antioxidant activity, antioxidant metabolite content, osmolyte content, and leaf mineral nutrient content were used to assess physiological responses to flooding. The hypothesis tested was that the six Prunus spp. rootstocks differ in their tolerance to flooding stress.
Section snippets
Experimental design and plant material
Twelve-month-old plants (time after grafting) of six different Prunus spp. cultivars: Flordaguard, Guardian, Nemaguard, P-22, R5064-5, and MP-29 provided by the USDA-ARS, Fruit and Nut Research Laboratory, Byron, GA were used as rootstocks. Flordaguard and Guardian were selected because of their importance in peach production in the southeastern United States. Nemaguard is an important rootstock for western peach production in the United States, MP-29 is a relatively new rootstock released for
Results
For all physiological variables, there was a significant statistical interaction (P < 0.05) between rootstock and flooding treatment on one or more measurement date. Also, there was a significant statistical interaction (P < 0.05) between rootstock and flooding treatment for several of the biochemical variables. Therefore, for all physiological and biochemical variables, differences between flooding treatments were analyzed separately for each rootstock, and differences among rootstocks were
Discussion
The mechanisms of response to flooding have not been elucidated in Prunus spp. and most research on this species has been based mainly on the effects of flooding on plant morphology (Gainza et al., 2015). The differences between Prunus spp. rootstocks that are sensitive or resistant to flooding have been described concerning the time it takes for symptoms to first be seen, recovery rate, and plant survival (Amador et al., 2012). Thus, it is necessary to validate the responses to flooding within
Conclusion
There was a significant difference among the six Prunus rootstocks tested in their ability to tolerate flooding stress. The rootstocks MP-29, P-22, and R5064-5 appear to be more tolerant of flooding stress than Flordaguard, the current standard rootstock for the subtropics. The sensitivity of Flordaguard to flooding stress confirms that alternative rootstocks are needed for subtropical areas that are prone to root zone flooding. Rootstock MP-29 is currently available to growers, whereas P-22
Author statement
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
CRediT authorship contribution statement
Trequan McGee: Formal analysis, Investigation, Writing - original draft, Project administration. Muhammad Adnan Shahid: Formal analysis, Investigation, Visualization. Thomas G. Beckman: Writing - review & editing, Resources. Jose X. Chaparro: Writing - review & editing, Resources. Bruce Schaffer: Writing - review & editing, Resources. Ali Sarkhosh: Supervision, Writing - review & editing, Resources, Validation.
Acknowledgment
The U.S. Department of Agriculture and the University of Florida Institute of Food and Agricultural Sciences are acknowledged for financial and material support of this study. Special thanks go to Dustin Huff and the stone fruit laboratories in the Horticultural Sciences Department at the University of Florida for their assistance during the experiment.
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