Journal of Cleaner Production 115 (2016) 362e365

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Journal of Cleaner Production

journal homepage: www.elsevier.com/locate/jclepro

Note from the eld

Exploring rhizospheric interactions for agricultural sustainability: the

need of integrative research on multi-trophic interactions
Rama Kant Dubey a, 1, Vishal Tripathi a, 1, Pradeep Kumar Dubey a, H.B. Singh b,
P.C. Abhilash a, *
a
b

Institute of Environment & Sustainable Development, Banaras Hindu University, Varanasi 221005, India
Department of Mycology & Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi 221005, India

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 28 March 2015
Received in revised form
20 December 2015
Accepted 21 December 2015
Available online 8 January 2016

Large scale exploitation of rhizospheric interactions is essential for enhancing the agroecosystems
resilience to climate change and also for adopting inventive adaptation strategies for maximizing the
food production under such adverse conditions. Successful exploitation of rhizospheric interactions can
be used for improving the soil fertility and organic carbon pool while minimizing the trace gases
emission from agrosystems. Most importantly, such knowledge can be used to enhance the plantmicrobe interactions, conferring diseases resistance to host plants, bioremediation and restoration of
marginal and degraded lands. However, recent studies proved that changing climatic conditions can alter
the rhizosphere biology by modifying the root exudation rate, resource availability and biogeochemical
cycling. Therefore, strategic and applied researches are essential to explore the rhizosphere biology
under changing climatic conditions and harnessing all benecial interactions as a low-input biotechnology for sustainable agriculture, ecosystem restoration and environmental sustainability.
2015 Elsevier Ltd. All rights reserved.

Keywords:
Rhizosphere biology
Climate change
Plant-microbe interactions
Sustainable agriculture

1. Introductory note
Plant-microbe interactions play a major role in sustainable crop
production including conferring disease resistance to crop plants
against a wide range of pathogenic organisms (Coninck et al., 2015)
through their specialized and customized chemical secretions
(Gourion et al., 2015; Bonfante and Genre, 2015). While their
defence strategies are at par with the arm and ammunition strategies of the modern world, there is a growing concern that climate
change (mainly due to elevated carbon dioxide (e-CO2) and temperature) can weaken the plant-microbe defence partnership
mainly by disrupting their chemical communication network
(A'Bear et al., 2014). Moreover, the increasing soil pollution due to
toxic chemicals is an additional threat to the chemical signalling of
plants and their associated microbiome. Though such communications error can cause a drastic impact on our biodiversity,
elemental and hydrological cycling and even global agricultural
production itself (Singh, 2015; Niles et al., 2015), still there are

* Corresponding author. Tel.: 91 9415644280 (mobile).

E-mail addresses: pca.iesd@bhu.ac.in, pcabhilash@hotmail.com (P.C. Abhilash).
1
Authors contributed equally.
http://dx.doi.org/10.1016/j.jclepro.2015.12.077
0959-6526/ 2015 Elsevier Ltd. All rights reserved.

many known unknowns and unknown knowns regarding plantmicrobe partnerships under adverse conditions. Therefore, the
present note is aimed to highlight the importance of harnessing
plant-microbe interactions for agricultural sustainability and the
impact of changing climatic conditions on plant adaptations and
interactions with pathogens, parasites, mutualists and chemical
pollutants.
2. Plant-soil-microbe and climate nexus
Maximizing the food production for a rapidly growing population is one of the immediate sustainability challenges of the 21st
century (Pretty, 2008; Dubey et al., 2016). Therefore, one of the
important arenas of harnessing plant-microbe partnership for human wellbeing is sustainable food production. However, the
changing climate can alter the phenology, reproduction, owering,
anthesis, pollen viability, pollination, seed lling duration, seed
setting, seed size, seed quality and yield of agricultural crops (Singh
et al., 2013). The warming climate and e-CO2 are found to lengthen
the growing season in plants (Reyes-Fox et al., 2014). Such
phenological shift can cause a great mismatch between plant and
insect pollinator population. Consequently, changes in interspecic
relationship of plants with its competitors, predators, parasites,

R.K. Dubey et al. / Journal of Cleaner Production 115 (2016) 362e365

symbionts and mutualists can modify the community structure and

ecosystem function. Plants can also respond to climate change by
shifting their climate niche. So the biodiversity would also be
affected by decrease in the level of genetic diversity of populations
due to directional selection and rapid migration, which could in
turn affect the ecosystem functioning and resilience (Bellard et al.,
2012).
While e-CO2 can enhance the plant growth up to a certain
extent, the increase in atmospheric CO2 together with other abiotic
stresses like temperature, drought, ozone, salinity etc will negatively affect the plant growth and yield (Abhilash et al., 2015). It is
also believed that warming climate may increase the yield of some
crops in colder areas of the planet (Lobell and Gourdji, 2012) provided that nutrient level, soil moisture, water availability, and other
conditions must also be favourable (Niero et al., 2015). In a highCO2 world, there will be decrease in N content that may reduce the
sink protein concentration (e.g., grains and tubers) and overall
decrease for most macro and micronutrients under e-CO2, in major
staple crops like maize, rice and wheat (DaMatta et al., 2010; Lobell
et al., 2013). Thus, the overall impacts of climate change on agriculture are expected to be negative, threatening global food security, most seriously affecting the agriculture and human well-being
of the already vulnerable and food insecure populations of the
developing and undeveloped world (Nelson et al., 2009; KabuboMariara and Karanja, 2007).
Apart from the issues of food security, the changing climate will
accelerate the disease prevalence in crops which in turn reduce the
crop yield and would necessitate the excessive use of pesticides and
fertilizers. Moreover, the warming climate can alter the mobility,
leaching, bioavailability, volatilization and global transport of
chemical pollutants from the agrosystem (A'Bear et al., 2014;
Tripathi et al., 2015) and will facilitate the enhanced bioaccumulation and biomagnications of pollutants in food chain.
Furthermore, it has been estimated that the warming climate will
reduce the fertile land area of maize and wheat by 6e23% and
40e45%, respectively, mainly due to the deciency of water (Singh
et al., 2013). Similarly, the change in rainfall pattern can affect the
productivity of the rainfed crops that are planted over the 60% of
the crop land area. The alteration in source to sink relation due to
the shift in the assimilate allocation between shoots and roots may
signicantly affect the production of tuber crops (Singh et al., 2013).
In the case of oil crops, the warming climate can also alter the oil
content, quality, meal protein and glucosinate levels (Barbetti et al.,
2012).
Another area of concern for the climate scientist is the climate
change induced shift in functional diversity of microorganisms.
Plants have strong effect on rhizospheric microbial community and
shape their composition in the rhizosphere due to the rhizodeposits which varies with plant species, plant age, location along the
root system and soil type (Mitter et al., 2013). While elevated CO2
will facilitate the plant growth and increase the soil carbon pool
through enhanced root exudation and litter addition, the dissolved
organic carbon (DOC) will be rapidly dissipate from the soil due to
enhanced volatilization. Increased microbial activities facilitate the
occurrence of extracellular enzymes like peptidases, chitinases and
phosphatases and will leads to the enhanced turnover of soil
organic matter (SOM) (Burns et al., 2013). Increased turnover of
SOM will enhance the N2 availability, however soil microfauna
mediated increased production of NO3  will also increase the
leaching of N2 from soil. Reduced water availability may decrease
the mineralisation and stabilisation of organic matter and minerals
in the soil (Carolin et al., 2014). In contrary to these, some studies
reported that elevated CO2, will reduce the N2 content and increase
the C:N ratio in plants. Increased lignin content of leaf litter will
slow down the rate of decomposition and could promote the

363

dominance of lignocellulolytic fungi in soil (A'Bear et al., 2014). The

reduced nutrient content of the leaf litter may make the nutritionally conservative fungal mycelia as alternative source of food
for soil invertebrates, affecting the fungal mediated decomposition.
Thus, changes in litter composition and consumption may alter the
structure of litter layer, soil surface and nutrient dynamics and
thereby differentially affecting the decomposers community,
composition, ecosystem regulation and carbon feedback. Still little
is known about the impact of climate change on belowground
community structure due to complexity of the below ground food
web (Abhilash and Dubey, 2014).
Apart from the changes in plant-soil nexus, changing climate
may alter the pathogen life cycle, expression of host resistance,
disease epidemiology and severity of disease epidemics, development of new races or pathotypes, virulence, overwintering or
oversummering of the pathogen etc. Warming could be favourable
for the pathogens like Verticillium longisporium, Sclerotinia sclerotiorum, Alternaria brassicae and Phoma lingam (Reyes-Fox et al.,
2014). Host specicity and mode of infection of the pathogen can
also be affected due to the change in biochemical and physiological
response of the host and the pathogen. Change in abiotic factors
such as elevated O3 level may favour necrotic pathogens, which
derive nutrients from killed host tissues. Although e-CO2 may boost
the plant health by enhancing the host resistance; however, an
increased plant canopy will offer additional infection sites for
pathogens. Thickening and deposition of wax over the leaf surface
will alter hostepathogen interactions whereas the changes in stomatal physiology will affect the pathogen invasion (Eastburn et al.,
2011; Prasch et al., 2014). Unfortunately, current studies are targeted towards the individual pathogen interaction with host plant
under the changing climate and there is a scarcity of information
regarding the interactions of host plants with multiple pathogens
under changing climatic conditions (Weyens et al., 2009; Vellend,
2010; Philippot et al., 2013; Saleem et al., 2014; Reyes-Fox et al.,
2014). Furthermore, agricultural scientists lack knowledge about
the shift in occurrence of various diseases under future climate
scenarios as prediction becomes much more complicated by the
uncertainty of adapted farming technique and crop genotypes under the changing climate.
3. Socio-economic dimensions of exploiting plant-microbe
interactions
A deep understanding of the plantemicrobe interactions will
leads to developing new generations of plant cultivars that have the
potential to grow under the stress of warming climate and elevated
CO2 (Philippot and Hallin, 2011). Importantly, such plant cultivars
can be customized for the cultivation even in degraded and marginal lands so that such kinds of lands can be successfully exploited
for the agricultural extensication without bringing new land into
cultivation practices and also preventing the subsequent loss of
biodiversity due to such land-use modications. Apart from that,
harnessing of plant-microbe interactions also offers societal benets such as healthy and nutritious food through bio-fortication
(Song et al., 2015) and help in postharvest management by
increasing the shelf life of agricultural produce (Ramos-Solano
et al., 2015). Therefore, unravelling of the rhizospheric interactions can offer solution to present and future challenges of
providing food, feed, fodder and biofuel requirements of a growing
population by sustainable agriculture practices. Benecial soil microorganisms can also offer substantial socioeconomic benets to
the global economy by reducing the dependency on synthetic fertilizers and pesticides while supporting various ecosystem functions and processes. Therefore, harnessing plant-microbe
interactions will not only help in climate change mitigation but also

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R.K. Dubey et al. / Journal of Cleaner Production 115 (2016) 362e365

Fig. 1. (A). Multiple stresses in plants under changing conditions and (B) signalling cascade in plants in response to multiple stresses (adapted from Prasch and Sonnewald (2014)).
Though the elevated CO2 is believed to have a fertilisation effect on plants, the increase in abiotic stress factors like temperature, drought, ozone, salinity will negatively affect the
plant health. According to Prasch and Sonnewald (2014), two protein kinase signalling complexes viz. Target of Rapamycin (TOR)-1 and Sucrose-non-fermenting-1 related protein
kinase (SnRK1) will balance the interplay between growth and stress response of plants. SnRK1 will be activated under the stress condition and will slow down the growth process
by activating the abscisic acid response element binding proteins (AREBPs). Moreover, the stress responsive hormones may trigger the downstream signalling cascade using
mitogen-activated protein kinases (MAPKs), Snf1-related kinases (SnRKs) and Ca2-dependent protein kinase (CPKs) cascades, which in turn initiate a reversible chain of protein
phosphorylation events. These signal transduction pathways lead to the activation of well-characterized proteins involved in biosynthesis of proteases, transporters, and chaperones
as well as osmoprotectants and detoxication enzymes. However, TOR-1 will be activated under the high nutritional condition to support the plant growth. These transcriptomic
changes show the regulation of novel genes affecting the synthesis of proteins and metabolites leading to change in photosynthesis, carbon metabolism, growth, amino acids,
sugars, starch synthesis and other metabolic processes. However, there is still a signicant knowledge gap regarding plant molecular responses to climate change catastrophes.
Though we are moving towards to answer most of these questions through the latest developments in omic technologies; still we are far behind from having a comprehensive
knowledge of the diverse molecular responses of plant tness to changing climate. (Figure drawn by Sheikh Adil Edrisi).

R.K. Dubey et al. / Journal of Cleaner Production 115 (2016) 362e365

strengthening the green economy for achieving economic stability

r et al., 2015).
(Schlo
4. Future perspectives for sustainable crop production
In future it is likely that plants and their associated benecial
soil fauna will be exposed to many of these abiotic or biotic stresses
in combination rather than isolation. Therefore, an integrated and
holistic understanding of rhizosphere biology is essential for the
maintenance and management of various terrestrial ecosystems
under adverse conditions (Fig. 1). Moreover, such knowledge can be
used for manipulating the rhizospheric systems for bioremediation,
biomass and biofuel production, soil carbon sequestration and
sustainable agricultural production. However, in order to exploit
the benecial interactions in rhizospheric zone, we need much
more emphasized transcriptomic, proteomic and metabolomic
studies to understand the regulation of novel genes, proteins and
metabolites affecting the photosynthetic processes, carbon metabolism, amino acids, sugars and starch synthesis in plants growing
under the multiple stresses and their interactions with microbiome. This will be helpful in gaining deeper insight into molecular
processes controlling the responses in plants and further shaping
the plant's ecological interactions under climate change. Importantly, a thorough understanding of the plant-microbe-soil and
climate nexus is essential to elucidate the survival and adaptation
of plants under changing climatic conditions and can be used to
modify the rhizospheric environment for sustainable agricultural
production.
Acknowledgements
Financial support from Science Engineering Research Board,
Govt. of India (No. SR/FT/LS-111/2011), and University Grants
Commission (No. F.41-1110/2012 (SR)) is gratefully acknowledged.
Rama Kant Dubey is thankful to CSIR for awarding Senior Research
Fellowship (CSIR-SRF).
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