Submitted to Land Degradation & Development
Continuous Cropping and
Natural Fallow Practices Affect Tobacco Fitness and Soil Microbiomes
Hao Jiang1,
Huanhuan Shao2, Quanju Xiang3, Yunfu
Gu3,
Bin Li4, Huizhan Gu4, Yu
Guan4, Yuanbin Zhang1
1Institute
of Mountain Hazards and Environment, Chinese Academy of Sciences,
Chengdu 610041, China
2 College of Life Sciences, Sichuan Normal University,
No. 1819, Section 2, Chenglong Avenue, Longquan District, Chengdu,
610101, China
3 Department of Microbiology, College of Resources,
Sichuan Agricultural University, Chengdu, 611130, China
4Sichuan
Branch of China National Tobacco Corporation, Chengdu 610000, China
Correspondence address:
Yuanbin Zhang
Institute of Mountain Hazards and
Environment, Chinese Academy of Sciences
Chengdu 610041, China
Tel: +86-28-85557542; Fax:
+86-28-85222258; E-mail: zhangyb@imde.ac.cn
Running title:Tobacco fitness and soil
microbiomes
ABSTRACT
Natural
fallow practice has been identified as an effective way to overcome
obstacles of continuous cropping. However, how the resulting soil
microbial changes impact plant fitness, and how the context-specific
differences diverge from those caused by continuous cropping remain
largely unknown. This study used the third-year continuous tobacco
cropping soil (CCS) and natural fallow soil (FS) to cultivateNicotiana tabacum . The influences of soil microorganisms on the
fitness of N. tabacum were assessed by reassembling soil
microbial communities. Then, the bacterial and fungal community assembly
of the bulk soil and the rhizosphere were characterized using amplicon
sequencing and statistical analysis. The results indicated that soil
microorganisms play more important roles for plant fitness for N.
tabacum grown in FS compared with CCS. Moreover, the abiotic context of
FS exerts stronger effects compared with those of CCS for the reassembly
of soil microbiomes. Comparative analysis identified the
context-specific microbial clades and the differential strength of
rhizosphere effects. In conclusion, this paper provides context-specific
microbial evidence, which may unravel the potential mechanism underlying
the different response of N. tabacum to changes of soil
microbiomes induced by natural fallow and continuous cropping practices.
KEYWORDS: continuous
cropping, plant fitness,
natural fallow,
rhizosphere effect,
microbial microbiome
1
INTRODUCTION
Climate change, human activities, and environmental pollution has
resulted in a series of adverse impacts, such as land degradation and a
shortage of agriculturally productive land, thus putting agricultural
production at risk. To achieve stable yields and continuous benefits, a
number of field- or cash-crops are often
continuously cropped, which is
combined with the intensive application of
fertilizers
by producers. As a result,
obstacles
to continuous cropping occur frequently, such as disruptions of soil
health, soil microbial community composition, and function (Garbeva et
al., 2004). These effects are often responsible for soil-borne disease
enrichment (Berendsen et al., 2012). However, a number of species may be
able to cope with successive changes of the soil microenvironment via
physiological adaptation (Teste et al., 2017; Hu et al., 2018). It has
been postulated that beneficial plant–microbe interactions might offer
promising strategies (Berg, 2009; Berendsen et al., 2012). An increasing
body of evidence confirmed that beneficial microbes can optimize plant
growth (Venkatachalam et al., 2014) and protect roots against microbial
pathogens (Bonanomi et al., 2018). For example, the flavobacterium TRM1,
found in the rhizosphere of species
resistant to the soil-borne pathogen Ralstonia solanacearum could
suppress disease development and enhance wilt resistance in tomato (Kwak
et al., 2018). Bacterial root commensals have been suggested to shape
fungal and oomycetal community structure and protect plants against
fungi and oomycetes, thus promoting plant survival (Duran et al., 2018).
However, knowledge of the microorganisms underlying the process and the
identity of beneficial microbes still remains unclear.
Soil microorganisms have been
confirmed to be involved in many key processes of the soil ecosystem
(Jansson & Hofmockel, 2020) and play key roles in
regulating
soil carbon dynamics (Zhou et al., 2012), nutrition cycling (Kuypers et
al., 2018; Luo et al., 2018),
and
the turnover of organic matter (Beulig et al., 2016; Xun et al., 2018).
Still, producers tend to ignore the
potential risks arising from changing soil microorganisms and focus more
on specific agricultural management practices (e.g., long-term
monoculture and fertilizer utilization) to achieve high
yields.
With regard to this situation, several productive and successful
agricultural practices, such as organic farming (Reganold & Wachter,
2016), no-tillage (Ashworth et al., 2017), and rotation (Liu et al.,
2019), have been applied and many crucial findings based on soil
microbiomes have emerged (Wang et al., 2017; Chen et al., 2018; Hartman
et al., 2018). However, the current shortage of labor seriously limits
these applications. Instead, conventional practices, such as
natural
fallow, are being widely used worldwide.
For
most crop plants, however, knowledge on the changes of microbial
communities under continuous cropping and natural fallow conditions
remains scarce. Moreover, the major contributors, particularly those in
rhizosphere microbiomes, to plant growth and soil health remain equally
elusive (Lau & Lennon, 2012; Venkatachalam et al., 2014; Bender et al.,
2016).
Nicotiana tabacum is a model
species of agricultural biotechnology and is very sensitive to
continuous cropping. This study hypothesized
that
the changes of soil microbial
community, especially changes of the specific microbial clades and
rhizosphere effects caused by the natural fallow practice, could enhance
plant
fitness.
To test our hypothesis, continuous
tobacco cropping soil (the third year) and natural fallow soil were used
to cultivate N. tabacumplants. First, the influences of soil microorganisms of both conditioned
soils on N. tabacum fitness
were assessed by reassembling soil microbial communities. Then, the
bacterial and fungal community assembly of the bulk soil and rhizosphere
were characterized. The aims of the
study were (i) to identify whether
changes of the soil microbiome, induced by natural fallow practice,
support a more diverse and active soil biota compared with changes
induced by continuous cropping practice, and would consequently enhanceN. tabacum fitness; and (ii)
to identify the context-specific
differences of microbiomes and rhizosphere effects caused by continuous
tobacco cropping and natural fallow practices.