Research article
Drought tolerant Ochrobactrum sp. inoculation performs multiple roles in maintaining the homeostasis in Zea mays L. subjected to deficit water stress

https://doi.org/10.1016/j.plaphy.2020.02.025Get rights and content

Highlights

  • PGPR Ochrobactrum sp. NBRISH6 improve overall plant health under abiotic stresses.

  • NBRISH6 inoculation modulates physiological and anatomical aspects in maize under deficit water stress.

  • NBRISH6 inoculation also maintains maize fitness by modifying metabolic and molecular facets under deficit water stress.

Abstract

Plant growth-promoting rhizobacteria (PGPR) improve plant health under various biotic and abiotic stresses. However, the underlying mechanisms of the protective effects of PGPR in deficit water stress (WS) remain less explored. This study aimed to characterize the role of Ochrobactrum sp. NBRISH6 inoculation on maize (Zea mays “Maharaja”) under WS conditions using multiple approaches such as physiological, anatomical, metabolic, and molecular. The effect of NBRISH6 inoculation using maize as a host plant was characterized under greenhouse conditions in deficit water stress. Results from this study demonstrated that NBRISH6 significantly lowered the expression of genes involved in the abscisic acid cycle, deficit water stress-response, osmotic stress, and antioxidant enzyme activity (superoxide dismutase, catalase, ascorbate peroxidase, guaiacol peroxidase, and polyphenol oxidase). Phytohormones, i.e. indole acetic acid (IAA) and salicylic acid (SA) levels, intercellular CO2 concentration, metabolites such as simple sugars, amino acids, aliphatic hydrocarbons, and the number of shrunken pith cells modulated in maize roots inoculated with NBRISH6. The NBRISH6 inoculation also improved the plant vegetative properties (root length, 33.80%; shoot length, 20.68%; root dry weight, 39.21%; shoot dry weight, 61.95%), shoot nutrients, xylem cells, root hairs, vapor pressure deficit (75%), intrinsic water-use efficiency (41.67%), photosynthesis rate (83.33%), and total chlorophyll (16.15%) as compared to the respective stress controls. This study provides valuable insights into mechanistic functions of PGPR in WS amelioration and promoting plant physiological response.

Graphical abstract

Morphological, physiological, biochemical, molecular, and ecological changes induced by Ochrobactrum sp. (NBRISH6) in maize (Zea mays “Maharaja”) under deficit water stress (WS) compared to only WS conditions. The lavender coloured arrows indicate increase/up-regulation, while the red arrows indicate decrease/down-regulation, with respect to control (non-NBRISH6 treated) maize.

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Introduction

Water-stress (WS) is a major abiotic stress globally and a secondary impact of climate change on plants in particular, of agro-ecosystems. Deficit water stress (hereafter WS) exerts immense pressure on plants at various scales of their physiology, anatomy and agronomic attributes. Due to this, agricultural crops that are much sensitive to the environment lose their capability to resist and succumb to death resulting in loss in crop production. Maize (Zea mays) is one such crop very susceptible to deficit water stress. Maize is cultivated widely from the Southern to the Northern Hemisphere, and from arid and semi-arid to humid and semi-humid areas (Haarhoff and Swanepoel, 2018; Chellamma and Pillai, 2016). The crop is used in several industrial applications and as animal feedstock (Campos et al., 2004). Unfortunately, maize production is severely affected by the deficit water stress condition (Dicko et al., 2018; Iqbal et al., 2018). The negative impacts of deficit water stress on maize have been investigated on physiological, biochemical, and molecular levels (Barbosa et al., 2018). These include reduced photosynthetic rate, decrease in leaf relative water content (RWC), cellular desiccation, formation of free radicals, lipid peroxidation, disturbed enzymatic activity, and protein oxidation (Hussain et al., 2019). Recently, Daryanto et al. (2016) using data-synthesis approach determined 39% of yield reduction in maize during 1980–2015 worldwide. Application of breeding and genetics technologies to counter abiotic stress conditions such as deficit water stress has not shown much improvement (from 1 × 109–3 × 109 kg ha−1) since 1960 (Gong et al., 2015). Previous reports have well established the role of Ochrobactrum sp. in plant growth promotion and deficit water stress amelioration as a single inoculant as well as consortium (Paulucci et al., 2015; Saikia et al., 2018). PGPR influence multiple physiological and morphological changes in plants, causing increased stress tolerance (Ullah et al., 2018, 2019; Misra et al., 2017). They modulate phytohormones IAA (Mantelin and Touraine, 2004), gibberellins (Cohen et al., 2009), ethylene (Glick, 2005), and cytokine-ABA level (Cohen et al., 2009) resulting in modification of root morphology, increased water and nutrient acquisition, decreased leaf transpiration, and improved osmotic stress tolerance (Bisht et al., 2019; Bresson et al., 2013; Mantelin and Touraine, 2004). Bacillus, Ochrobactrum, and Pseudomonas spp. reduce antioxidant enzyme activity (APX, CAT and GPX) and cause higher accumulation of osmolytes (proline) and sugars in plants with an eventual increase in plant biomass, relative water content, leaf water potential, and root adhering soil/root tissue ratio under WS conditions (Misra et al., 2019; Tiwari et al., 2016; Naseem and Bano, 2014; Vardharajula et al., 2011; Bano and Fatima, 2009). Further, they produce alginate, a chief EPS (exopolysaccharide) (Halverson, 2009) that maintains hydration of formed biofilms, attenuates oxidative stress, and increases aggregation of stability and RAS/RT (root-adhering soil/root tissue) ratio, leads to increased uptake of water and nutrients for plants under WS (Vardharajula et al., 2011). PGPR also possess activities such as siderophore production, nitrogen fixation, and phosphate solubilization and ability to chelate, fix and solubilize elements to influence the rhizospheric ecology as well as recycling of soil nutrients that are crucial for soil fertility (Mishra et al., 2017; Abiala et al., 2015; Redmile-Gordon et al., 2014; Qurashi and Sabri, 2012). Several studies have focused on plant performance as an outcome to understand plant-bacteria interactions (Mussa et al., 2018; Mishra et al., 2017; Abiala et al., 2015; Redmile-Gordon et al., 2014; Bresson et al., 2014, 2013; Vardharajula et al., 2011). Recently, Khan et al. (2019) evaluated the effect of PGPR on the physiology of chickpea grown in drought stress conditions and correlated them with the metabolic profiling in leaves of chickpea exposed to deficit water stress. However, a comprehensive study of PGPR effect on morphological, physiological, biochemical, metabolic, and molecular aspects under WS conditions is lacking. Therefore, an attempt has been made with a multidisciplinary approach, involving morphological, physiological, biochemical, metabolic, and molecular analyses to understand the plant response to deficit water stress under NBRISH6 treatment in a holistic manner. To our knowledge, no other interaction study between maize and Ochrobactrum sp. under WS conditions encompassing multiple approach has been performed earlier. This study shall improve our discernment on plant growth promotion and stress tolerance mechanisms in a plant-microbe interaction system under stressed environments.

Section snippets

Bacterial strain and its growth condition

The bacterial strain NBRISH6 (Accession. No. KP300814) used in this study was isolated from an extreme environment of nearby locations of volcanos in Andaman and Nicobar Islands (12°07′N 92°47′E), India (Mishra et al., 2017). PGP attributes of NBRISH6 are listed in Table S1. For preparing bacterial culture, NBRISH6 was inoculated into nutrient broth (NB) medium at 28 °C under constant shaking of 180 rpm for 48 h. NBRISH6 was previously characterized for plant growth promoting traits and abiotic

NBRISH6 promotes growth and enhances the nutrient content of maize

Inoculation of NBRISH6 has significantly increased the growth and nutrient accumulation in maize plants (Table 1 and Supplemental Fig. S1). Overall the plant growth parameters, i.e., shoot and root length (SL and RL), shoot and root fresh weight (SFW and RFW), shoot and root dry weight (SDW and RDW), number of leaves per plant (NLPP), and leaf diameter (dia) recorded and found a significant increase as compared to their respective controls under normal and WS condition. Significant reduction

Discussion

Plant growth promoting effects of Ochrobactrum sp. have been well established in earlier studies (Mishra et al., 2017; Meng et al., 2014; Imran et al., 2014). Findings in the present study in relation to effect of NBRISH6 inoculation on plant corroborates with the results of previous study (Chakraborty et al., 2013) where Ochrobactrum sp. significantly enhanced shoot and root biomass under WS conditions. Moreover, regarding nutrient status, results of the present study were in agreement with

Conclusion

This study shows that PGPR promotes plant growth under WS by various mechanisms including improving vegetative growth, nutrient uptake, photosynthetic parameters, root anatomical features, lowering oxidative stress, phytohormone level, metabolite accumulation and expression of genes of antioxidant enzymes, phytohormones and deficit water stress-response genes. This multidisciplinary approach may improve the understanding of PGPR mediated protection and plant growth promotion under deficit water

Author contribution statement

PSC conceived the idea, and co-ordinated the research. SKM, MHK, SM, VKD, SG, ST, SCG conducted experiments and analyzed the data. SKM, MHK, SM, and PSC wrote the manuscript. All authors read and approved the manuscript.

Declaration of competing interest

The authors declare that they have no conflict of interest.

Acknowledgements

Authors acknowledge Director, CSIR-National Botanical Research Institute for providing facilities and support during the study. The authors acknowledge the financial assistance from CSIR-Network project (MLP022) and In-house project OLP105. Authors have no conflict of interest.

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