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.