Timing of water use and phosphorus exploitation strategies are promising key traits of Sorghum to maintain biomass and yield production under resource limitations

doi:10.21203/rs.3.rs-4346438/v1

Aims

Limited access to nutrients and water is leading to yield losses in smallholder farming systems in semi-arid regions. Therefore, crop rotations including legumes as well as utilizing drought-tolerant sorghum varieties might be a strategy to improve access to scarce resources.

Methods

Two early and five late maturing sorghum genotypes were tested to identify stress adaptation traits to water and phosphorus limitations in combination with or without ¹⁵N labelled legume pre-crops on a phenotyping platform.

Results

Lower soil P content significantly delayed the time of flowering of all genotypes compared to higher P content, however organic residues could reduce this effect. ¹⁵N recovery in sorghum biomass proved the use of pre-crop root residue N in all treatments, although there was only a beneficial pre-crop effect on sorghum biomass and yield under sufficient water supply. Mycorrhizal infection was relevant for plant nutrition at anthesis under low P and showed a positive correlation with ¹⁵N recovery and root P content. Drought had the major impact on yield. Early maturing genotypes, with the highest reduction in shoot biomass and adapted transpiration prior flowering, could maintain yield production.

Conclusions

A promising trait combination for nutrient-poor soils in semi-arid areas with high drought risk, seemed to be early-maturing varieties with a high root to shoot ratio, rapid AMF establishment and low transpration (normalized to leaf area T_n) – in this study realized in the early maturing genotype Grinkan. Such genotypes save water prior flowering and reduce their post flowering water stress in combination to their P uptake withstanding low soil availability.

Drought

multiple resource limitations

phosphorus

plant pehnologcial development

sorghum

water use

Crop production in semi-arid (sub-)tropical regions is prone to water scarcity (Rockström and Falkenmark, 2015) and very often coupled with a low soil fertility (Sahrawat, 2016). Climate change affects agriculture worldwide through warming, changing precipitation patterns and more frequent extreme weather events such as prolonged drought periods. According to future climate projection many semi-arid regions will become even drier (Huang et al., 2016) and, in conjunction with land use activities, soil degradation will further increase further reducing the land area suitable for crop production (Saco et al., 2018). At the same time, the global population continues to increase with strongest growth projected for sub-Saharan Africa, where population is estimated to exceed 2 billions by 2050 (United Nations, 2019). In order to maintain food security and environmental resilience, sustainable agricultural practices are essential. The implementation of legume crop rotations in combination with drought adapted staple crops such as sorghum can harness numerous benefits, including soil health, crop productivity and reduced environmental impacts (Franke et al., 2018).

Subsistence farmers in the semi-arid regions in Africa and Asia grow sorghum (Sorghum bicolor [L.] Moench) for consumption (Murty et al., 2007). It is the fifth most important staple crop in the world (FAO, 2023). Apart from human nutrition, sorghum is cultivated for livestock fodder (Ronda et al., 2019), bioenergy production(Rooney et al., 2007) and the production of traditional beverages in some regions of Africa (Belton and Taylor, 2004). Sorghum is an annual short-day member of the family Poaceae, which originates from Africa and is predominantly self-pollinating. With a C4 photosynthetic pathway, and a thick wax leaf layer sorghum is adapted to semi-arid conditions (Hariprasanna and Patil, 2015). In India, sorghum cultivation in the post rainy season is a common practice, thus the stored soil moisture needs to meet the plants water demand for the whole growing season (Kholová et al., 2013). Although sorghum tolerates drought conditions more than most other crops, water stress causes the highest yield losses, specifically under such cultivation conditions (Assefa et al., 2010). Drought can occur at all crop development stages and, therefore, causes many complex plant responses which cannot be jointly targeted within one breeding program (Passioura, 2012). The adaptation mechanisms and their traits can be categorized into drought avoidance, escape and tolerance and summarize diverse morphological and physiological adaptation patterns (Fang and Xiong, 2015). Particularly, conservation and efficiency of water use are related to how biomass production is adapted to soil moisture availability under water scarce conditions (Passioura, 2012). Soil water conservation traits can be estimated by transpiration rates normalized to leaf area (Karthika et al., 2018). Early flowering (Abraha et al., 2015), fast maturity and plasticity of leaf area development are characteristics of drought adapted sorghum varieties (van Oosterom et al., 2011). The high genetic diversity of sorghum for early and mid-season drought stress adaptations(Reddy et al., 2008a) facilitates the development of more resilient and adaptable varieties to meet the challenges of drought-prone environments.

Apart from the water deficit, use of mineral fertilizers is very limited in smallholder farmers’ crop production systems. Mainly cash crops are fertilized during the rainy season, while sorghum is mostly grown in the post or the short rainy season with low or no inputs in India(Anbazhagan et al., 2019) and sub-Saharan Africa (Weltzien et al., 2018). However, typical soil types like Alfisols have a low amount of organic matter and plant available nutrients (Selvaraju, 1999; Sharma et al., 2005), especially plant-available phosphorus (P) (Nziguheba et al., 2016). Thus, crop rotations with legumes are a common practice and due to their ability to fix atmospheric nitrogen the use of nitrogen fertilizers could be partly reduced. Across agro-ecological zones legume crop rotations increased significantly cereal yields of maize, sorghum and millet, although the response of sorghum and millet was less pronounced compared to maize (Franke et al., 2018). In particular, subsistence farmers rely on affordable management practices. In that context, legume crop rotations not only affect productivitiy of crop rotations but also farmers’ revenues, as expensive nitrogen fertilizers can be substituted. After legume biomass is harvested, their decomposing root residues and the respective root channels serve as nutrient, organic carbon and microbial activity hotspots (Pankhurst et al., 2002). Further implications on soil health and nutrient cycle after legume cropping could be observed, as lower infection rates with striga (Franke et al., 2018), enhanced mycorrhizal infections and increased phosphatase activity resulted in higher N and P contents of the subsequently cultivated sorghum (Alvey et al., 2001).

To identify the direct contribution of the preceding legume root residues to the nutrition of the main crop, single plant isotope labeling (Götz and Herzog, 2000) can be used to measure the ¹⁵N rhizodeposition of legumes into the soil and the subsequent uptake rate (Fustec et al., 2010).

Sorghum cultivation in semi-arid regions is affected by water shortage and low plant available P which both can causes decreased sorghum yields (Leiser et al., 2012). Thus, an evaluation of the performance of different sorghum varieties under multiple resource limitation is essential for a significant identification of the varieties’ breeding potentials. The variety M35-1 is a popular variety grown in the post rainy season in India because of its’ stable yield performance under terminal drought conditions (Reddy et al., 1988). M35-1 often serves often as a control variety in germplasm studies to identify new accessions or breeding progress of genotypes under unfavorable water and nutrient conditions. It also serves as genetic source for new breeding cultivars or hybrids (Reddy et al., 1988; Reddy et al., 2009) and, thus, was used as control in our study.

To acquire knowledge about specific sorghum traits which mitigate stress under multiple resource limitations a four-factorial experiment was conducted with two water-levels, two P-levels, two ¹⁵N-sources and five sorghum genotypes. The study aims were (i) to examine the performance of early and late maturing sorghum genotypes (ii) to measure if different soil P contents have an influence on water-stress mitigation, (iii) to determine whether nutrient uptake from mineral fertilizer or organic residues may have a positive influence on sorghum’s nutrient status and water uptake performance, especially under resource limitations. Resulting hypothesis were that (i) early maturing genotypes perform better under water limiting conditions, (ii) that a higher P availability lead to yield increase under drought conditions, (iii) that genotypes which use the legume residues nutrient reservoir have an improved nutrient supply which leads to higher biomass and yield production, especially under concomitant P and water limitations.

2.1 Soil parameters

The soil originating from the ICRISAT station was filled in the tubes with a bulk density of 1.4 g cm^− 3 (Vadez et al., 2008). The soil texture consisted of 17% silt, 21% clay and 62% sand and was identified as Alfisol. Plant available volumetric water content was 25.71%.

The initial Olsen P levels of the Alfisol ranged between 2 (Seetharama et al., 1984) and 7.1 mg P kg^− 1 (Sahrawat et al., 1995) and was used for the low P treatment without further P fertilization. In contrast, the tubes of the high P treatment received continuous P fertilizer since the establishment of the experimental set up. The same soil type was used for all treatment combinations and further soil characteristics differing with the P treatments are shown in Table 1.

Table 1

Soil characteristics
P level	OC	TN	pH	TP	P fractions
					NaCl HCL	NaHCO₃	NaOH	HCl	Residual P
	[%]	[%]		[mg kg^− 1]	[%]	[%]	[%]	[%]	[%]
high P	0,440	0,040	5,5	318,8	13,42	32,98	27,72	5,14	20,74
low P	0,544	0,051	6,1	100,8	0,68	2,57	31,92	3,20	61,63

2.2 Experimental set up

The experiment was conducted at the lysimetric phenotyping system of the International Crop Research Institute for the Semi-Arid Tropics (ICRISAT India, 17°31'03.6"N and 78°16'36.0"E) from July 2018 to February 2019. Detailed plant development records as well as plant specific transpiration measurements were possible on a single plant basis. A detailed description of the study area and facility setup is provided by Vadez et al., (2008). Briefly, semi-field conditions were created by placing cylindrical tubes (height 120 cm, diameter 25 cm) in a trench, thus a planting density of approximately 16 plants m^− 2 was reached. The open facilities had the possibility to prevent additional watering during rainfall events with a mobile shelter. During the sorghum cropping period in the post rainy season, the maximum and minimum temperatures ranged from 19.2–33.6°C to 5.2–23°C, respectively. In this study a four-factorial randomized split-plot design with soil P content (high and low P), water levels (well-watered and water stressed), N source (cowpea root residues and mineral fertilizer) and five sorghum genotypes was used. The tubes were placed in four blocks in separate trenches, with the factor combination P x water level. For the well-watered (WW) treatment, the water content was maintained at approximately 80% plant available water holding capacity (paWHC), while under the water stressed (WS) treatment 30% paWHC was the threshold for water addition. Each P and water-level combination was subdivided in two N source treatments. The different N sources were either ¹⁵N labelled root residues from the pre-crop cowpea [Vigna unguiculata L. Walp.] grown in the same tubes followed by sorghum cultivation or ¹⁵N labelled mineral fertilizer. Pre-crop cultivation and labelling procedures are explained in section 2.3. In total, five sorghum genotypes [Sorghum bicolor (L.) Moench] were grown, with two early maturing (Lata 3, Grinkan) and three late maturing genotypes (CSV14R, Keslapoor, M35-1), while M35-1 served as the control variety.

Five replicates per treatment combination resulted in total 200 tubes, i.e. sorghum plants, and is referred to as the main experiment. In order to get affordable information about belowground sorghum root traits and the plant development, an additional set of smaller tubes was used, with the same height (120 cm) as in the main experiment, but with a smaller diameter of 16 cm. Destructive sampling was conducted to get biomass data at stem elongation (36 DAS), anthesis (56–70 DAS) and maturity (105–112 DAS). This subset of tubes for destructive harvest was grown solely on soils, where previously pre-crops were cultivated, to be able to detect a potential re-use of legume root channels by Sorghum roots and exposed to both treatments – water and P levels. In total, additional 60 tubes, located in the same trench, were used for root parameterization. Although the biomass production in the smaller tubes was reduced to around 24% compared to the bigger tubes, we assume that, other morphological traits (as root biomass) changed proportional to the plant size and that physiological traits were not affected (see section 3.4). Furthermore, the flowering time point (DAS 54–71), physiological maturity (DAS 105–112) and genotype-specific patterns in development and biomass accumulation were identical for the sorghum plants in the tubes for destructive harvest comparable to the plants in the main experiment.

The main experiment results should provide detailed information about the treatment effects on morphological and physiological traits of the sorghum genotypes, while the extra harvest should link the above and belowground interactions to the quantified parameters.

2.3 Cowpea cultivation and ¹⁵N labeling

The pre-crop cowpea grew from July to September 2018. Five cowpea seeds (genotype: Giant Russian) were sown and the plants were thinned out to one plant per cylinder. Throughout the cultivation period the plants were irrigated sufficiently and pesticide and fertilizer application (except for P in the low P treatment) was conducted according to common practice. The cowpea plants were labelled with a ¹⁵N (99 atom%) tracer solution mixture of di-ammonium sulfate ((¹⁵NH₄)₂SO₄) (Cambridge Isotope Laboratories Inc., USA) and potassium nitrate (K¹⁵NO₃) (ISOTEC INC., USA). Five gram of the N fertilizer mixture with equal ¹⁵N proportions were diluted in 2 ml distilled water. The injected dose per plant and labeling event was approximately 30 µl. The tracer solution was injected bi-weekly until harvest into the plant stem with 10 µl GC-needles (SYR FN 50 mm Ga 26, Bevel Tip, Thermo Fisher Scientific, USA) according to the method by Götz and Herzog (2000) until the tracer solution was depleted. The continuous tracer application was performed to ensure a homogenous δ¹⁵N distribution within the cowpea plant organs. The aboveground biomass was harvested and dried at 60°C, weighed and milled at the lab facilities of the department of crop physiology at ICRISAT (Hyderabad, India). The remaining tubes without the pre-crop received 5 mg of mineral ¹⁵N tracer as (¹⁵NH₄)₂SO₄, diluted in 1 L H₂O after 31 days of sorghum sowing (DAS) and 7 days after soil saturation to prevent leaching of the ¹⁵N tracer and ensure plant uptake. 34 additional tubes were not labelled to estimate natural abundance δ¹⁵N values of cowpea and sorghum plant parts.

2.2 Sorghum cultivation

Six sorghum seeds of each genotype were sown on 19th of October 2018. Additional sorghum plants were grown in pots surrounding the trench to minimize border effects and pest control was applied according to common practice. From November 2018, Carbofuran (2,2-Dimethyl-2,3-dihydro-1-benzofuran-7-yl methylcarbamate) was regularly sprayed against the fall armyworm (Spodoptera frugiperda) and prevented successfully biomass loss. Fertilizer was applied according to soil P treatment before sowing. Low P big tubes received 2.3 g (low P small tubes 1.4 g) urea as N fertilizer and high P big tubes 5 g (high P small tubes 3.1 g) di-ammonium phosphate (DAP) to apply both, P and N. At 25 DAS, the 5-leaf stage, plants were thinned to one plant per cylinder, followed by soil saturation at DAS 27. Afterwards, plastic sheets and a layer of 2 cm polyethylene beads were placed on the soil surface to prevent about 90% of soil evaporation. Two days later, no more leaching was detected and the initial weight for the individual calculation of 80% field capacity per cylinder was recorded and served as reference weight for further calculations of the targeted water content (Vadez et al., 2008). Weekly weighing ensured the controlled water content monitoring and water was added in order to maintain the water levels of 80% or 30% paWHC. Sorghum was harvested during first half of February 2019 after reaching physiological maturity. The individual plants were separated in leaf, stem, panicle, tiller and tiller panicles, oven-dried at 60°C and weighed. After threshing, grain weight and thousand grain weight (TGW) was recorded. The samples were milled separately at the lab facilities of the department for crop physiology at ICRISAT and subsamples were sent to the University of Goettingen, for further lab analyses. Harvest time points of the extra harvest were selected based on the plants’ development status (stem elongation, anthesis and maturity), while the sample preparation was equal to the above mentioned procedure. In addition, root biomass was washed, collected with sieves, and stored in 70% ethanol until root scanning was completed. A small subsample was immediately frozen at -20°C for mycorrhiza estimation. After crown root counting, roots were oven-dried and milled.

2.3 Field measurements

Plant development was recorded bi-weekly with the following parameters: plant height until the last developed leaf, number of developed leaves, number of developing leaves, number of senesced leaves as well as tiller numbers and height. A developed leaf was counted when the lamina was fully unfolded at the stem. Senesced leaves were characterized by over 50% dried out, yellowish or dead appearance. Leaf area was measured at all green, developed leaves from the fifth leave upwards of all plants including tillers. The leaf area of the first four leaves was negligible and was therefore not measured. Total leaf length was measured from the separation point at the stem until the tip of the leaf, and the width at the widest point of the leaf. Calculation of leaf area was obtained by multiplying the product of leaf length and width with the shape correction factor 0.75 (Stickler et al., 1961). After emergence of the first flower, the flowering date was recorded daily and determined when more than 50% of the panicle was covered with anthers. Flowers were covered with light nylon bags to prevent damage by animals.

2.4 Analysis and calculations

For further analysis, the cowpea and sorghum plant samples were dried at 60°C and ground to a fine powder in a ball mill (MM200 Retsch Haan Germany). Three to five mg of the plant samples were weighed into tin capsules (IVA, Meerbusch, Germany) for the determination of δ¹⁵N isotope ratios, as well as N and C contents at the elemental analyzer (Flash, ThermoFisher Scientific, Bremen, Germany) coupled to an isotope ratio mass spectrometer (IRMS) (Delta Plus Conflo III, ThermoFisher Scientific, Bremen, Germany). The analyses were conducted at the Centre for Stable Isotope Research and Analysis (Georg August-University Goettingen).

As cowpea roots remained in the soil, the at% ¹⁵N values of cowpea aboveground biomass were used for further calculations and equal ¹⁵N enrichment of above and belowground cowpea biomass was assumed, due to the frequent labelling events occurring during the entire growth period. For calculating the remaining ¹⁵N tracer in the soil from the labelled cowpea root biomass, the root to shoot ratio of the cowpea genotype Giant Russian was estimated with 0.16 (Dwivedi et al., 2003). The remaining nitrogen in soil derived from cowpea root residues (TN_Croots) was calculated by the following Eq. 1.

\({TN}_{Croots} ={C}_{A}\left(g\right)*{N}_{fraction}*0.16\) Eq. 1

with C_A (g) as the cowpea aboveground biomass dry weight (DW), N_fraction as the fraction of N in the cowpea aboveground biomass and the coefficient 0.16, which subsequently could be multiplied to calculate TN_Croots, the amount of total N remaining in the soil from the cowpea root residues.

The sorghum N amount taken up (N_uptake) from either cowpea root residues or mineral tracer was calculated by multiplying the amount of N in the sorghum biomass (N_Blab) with the ¹⁵N fraction derived from the tracer pool, which can be gained by the isotope mixing model according to Eq. 2:

\({N}_{uptake} =\frac{{at\% ¹⁵N}_{Blab}-{at\% ¹⁵N}_{Bnat}}{{at\% ¹⁵N}_{tracer}-{at\% ¹⁵N}_{nat}}*{N}_{Blab}\) Eq. 2:

with at% ¹⁵N_{Blab/Bnat/tracer/nat} as the at% ¹⁵N of the labelled (Blab) and non-labelled (Bnat) sorghum plant biomass and the applied tracer pool from mineral or organic sources.

The input output ratio of the applied ¹⁵N sources was determined as sorghum N_recovery (%, i.e. the percentage of the N uptake from the provided tracer N amount (TN_tracer) from either mineral or organic (TN_Croots) source according to Eq. 3:

\({N}_{recovery} \left(\%\right)=\frac{{N}_{uptake}}{{TN}_{tracer|Croots}}*100\) Eq. 3

Total N (TN) content was calculated by the N fraction multiplied by the biomass (g) of the plant parts and the sum resulted in total biomass N content. Total P content was extracted by the nitric acid pressure digestion method (Heinrichs et al., 1986) and was measured on an inductively coupled plasma optical emission spectrometer (ICP-OES, Thermo Scientific iCap 6000 Series).

The weekly transpiration (L week^− 1) was estimated by calculating the weight difference between the weights of two successive weeks plus the added irrigation water (Vadez et al., 2008). Consequently, the total transpiration was the sum of all weekly transpiration values from initial weighing until harvest. The quantification of the normalized transpiration rate per unit of leaf area (T_n) allows an easy and non distructive assessment of the sorghum varieties transpiration characteristics throughout the plant development. T_n is defined as unit transpiration (L week^− 1) per unit of leaf area (m²) (Karthika et al., 2018).

Another parameter estimating the plant’s water use pattern during the growth period is the fraction of transpired water till flowering (FTWF). FTWF is calculated by dividing the cumulative transpiration (L plant^− 1) until flowering by the total transpiration (L plant^− 1) until harvest.

The water use efficiency (WUE) is defined as the unit grain DM (g) per unit water transpired (L) (Vaux Jr and Pruitt, 1983).

Root colonization with arbuscular mycorrhiza fungi (AMF) was determined by the modified root staining method (Vierheilig et al., 1998). Roots with approx. one cm length were heated in 10% KOH, stained with a 5%-ink-vinegar solution and stored afterwards in glycerol at 4°C until AMF was counted. AMF colonialization was determined by a modified root segment ± method (Nicolson, 1955) with the AMF colonization per root area. Therefore, a light microscope (Olympus BX40 with Olympus CMOS-camera SC50M) with a magnification of 150x (Olympus Ach 10x/0.25 ph ∞ 0.17, ocular 15x, Olympus Europe SE & Co. KG, Hamburg, Germany) in 4.9 Mpx resolution was used. AMF structures were clearly visible without any filter use and pictures were saved as TIFF with JPEG compression. Further counting process was conducted by the software tool ‘Fungi Tagger’ (https://gitlab.gwdg.de/sstock1/fungi_tagger) (Stock et al., 2021). The remaining washed roots scanned with a flatbed scanner and the image analyzing software WinRHIZO 2013e (Regent Instruments Inc., Québec, Canada) was used for root trait analysis. Root length (Rlength) (cm), root surface area (SurfArea) (cm²) and specific root density (SRD, cm g^− 1), with SRD being calculated by dividing Rlength (cm) by the root mass (g). Mycorrhized root area was the factor of the root surface area multiplied with the mycorrhiza infection portion.

2.5 Statistical Analysis

Data preparation and outlier elimination was performed using Microsoft.Excel (Version 16.29.1). Statistical analysis and graphical visualization were conducted using R.Studio (Version 4.2.2). Shapiro-Wilk test and Levene’s test were performed to check data for normal distribution and homogenous variances, respectively. If necessary, data were log transformed in order to fulfill the assumptions and an analysis of variance (ANOVA) was performed followed by a Tukey post hoc tests. For non-parametric data, the Kruskal-Wallis test was carried out followed by a Dunn’s post hoc test to identify statistical differences between groups. Significant differences were detected at a threshold of p < 0.05. The corrplot function of R was used to perform the Spearman’s rank correlation coefficient test with a threshold of p < 0.05.

Table 2 Mean sorghum parameters after the additional destructive harvest time points (stem elongation, anthesis and maturity). Root to shoot ratios, Mycorrhization and shoot P content the early and late maturing genotypes are shown. Significance letters show significant differences (p< 0.05) between growth stages, while the asterisk indicate significant differences between the early and late maturing genotypes within one growth stage (not significant (ns), 0.05, 0.01, 0.001; ns, *, **, ***).

Root to Shoot ratio

Mycorrhization (%)

Shoot P (mg g-1)

Development

early

late

WW

WS

Stage

early

late

High P

Low P

High P

Low P

High P

Low P

High P

Low P

Stem Elongation

0.21

a

0.15

a

ns

3,50

a

6,14

ab

ns

2,39

a

5,98

a

ns

3,29

b

2,01

b

***

-

Anthesis

0.44

b

0.27

ab

***

5,01

a

13,53

b

*

13,12

b

9,77

a

ns

2,8

b

1,71

ab

ns

2,76

a

1,6

a

*

Maturity

0.28

ab

0.30

b

ns

9,26

a

3,34

a

ns

11,96

ab

17,32

a

ns

1,22

a

0,87

a

*

2,08

a

1,23

a

*

n=8

n=12

n=4

n=6

n=5

3.1 Sorghum biomass and grain yield

Sorghum shoot biomass production was dependent on genotype (p = < 2.2^e − 16), P level (p = 6.409e^− 12), water availability (p = < 2.2^e − 16), N sources (p = 1.129^e − 06) and their interactions (Supplement, Table 1). The factor combinations P level x water level x N source resulted in a significantly higher biomass production of the late maturing genotypes compared to the early maturing genotype Grinkan (14.5–43.2 g plant ^− 1), while the second early maturing genotype Lata 3 (22.7–69.2 g plant ^− 1) had either a similar shoot production as Grinkan or an intermediate shoot production between Grinkan and the other late maturing genotypes. M35-1 produced the highest biomass with 105 g plant^− 1 ± SE 13.3 under well-watered conditions and supplied with high P levels and the organic N source. However, there was no significant decrease of biomass within the P levels under sufficient water supply, as well as at higher P levels under WS. Only under the combination of both abiotic stresses, low P and drought conditions, M35-1 showed a significant biomass reduction with 43.9–51.5 g plant^− 1, with a positive trend from mineral to organic N sources. The genotype CSV14R showed a similar response of shoot biomass to water and nutrient availability as M35-1, but with overall lower biomasses, ranging between 36.6–85.2 g plant^− 1. The biomass production of Keslapoor S ranged between 49.1–82.5 g plant^− 1. A genotype independent trend was the interaction between P level and N source (p = 0.001), as well as between P, water level and the N source (p = 0.004), whereby at WW conditions a positive influence of organic N sources from pre-crops on biomass production could be identified as statistically significant. However, under WS organic N sources had a positive effect on plant biomass production under low P. Vice versa, there was no or even a negative effect of organic N provision via pre-cropping under high P conditions on sorghum biomass production. There was no interaction between genotype and P level, but between genotype and water level (p = 0.02). However, the interaction between genotype, P and water level (p = 0.001) was highly significant (Fig. 1; Supplement, Table 1).

Sorghum yield production was mainly influenced by the water availability and drought had an overall negative effect on most of the P x N source x genotype combinations (Fig. 2). In fact, only Lata 3 could maintain yield levels (14-22.5 g plant^− 1) under high P irrespective of N sources or water levels (Supplement, Table 2). The genotypes Grinkan and M35-1 showed a negative trend in yield production under a high P supply and mineral N sources under WS, but it was not significant (Supplement, Table 2). Regarding the influence of P levels and N sources on yield, it has to be differentiated between water levels and genotypes. On average over all genotypes, the yield production under WS and mineral N sources was significantly higher when supplied with high levels of P compared to the low P treatment (p = 0,03), while under WW and organic residues as N source, there was no significant effect of P limitation (Supplement, Table 6). Under WW conditions P levels had no influence on grain yield, while under WS only Keslapoor S and Lata 3 displayed a significant yield decrease from high to low P levels (Supplement, Table 3). Organic N sources had a positive effect on yield production for the genotype Grinkan under both water and P levels, but this effect was only statistically significant under WW and high P (Supplement, Table 4). Lata 3 showed a trend for higher yields with organic N sources under low P and WW conditions compared to mineral ones. In contrast, Keslapoor S and M35-1 showed under high P and WW conditions a trend for higher yield production when supplied with organic compared to mineral N sources. In contrast, pre-cropping and the respective organic N sources reduced the yield production of CSV14R significantly under drought conditions for both P levels (Supplement, Table 4). Comparing the yield production between the genotypes, highest yields were achieved by CSV14R (44 g plant^− 1), Keslapoor S (43.5 g plant^− 1) and Grinkan (47.7 g plant^− 1) under high P availability and sufficient water supply. Also under WS conditions Grinkan was most productive genotype with 11.7–17.8 g plant^− 1, followed by Lata 3 with 2.48–21.7 g plant-1 and CSV14R when supplied with mineral N with around 7 g plant^− 1. Keslapoor S and M35-1 produced almost no yield under drought conditions (Fig. 2).

3.2 Utilization of organic and mineral nitrogen sources by sorghum

3.3 Utilization of Water Resources

The main factor affecting FTWF was the available water content. Under WS conditions all genotypes had a significantly higher FTWF compared to WW conditions (Fig. 4). Under WS the early maturing genotypes Grinkan and Lata 3 had FTWF values between 0.53–0.76 and 0.64–0.82, respectively, while the FTWF of the late maturing genotypes CSV14R, Keslapoor and M35-1 ranged between 0.76–0.86, 0.87–0.90 and 0.86–0.89, respectively. Under ample water supply, all genotypes except Lata 3 had higher FTWF values at low P (mean 0.45 ± SE 0.018) compared to high P (mean 0.38 ± SE 0.011) conditions. However, CSV14R, Keslapoor S and Grinkan reduced significantly the FTWF under low soil P availability when supplied with organic residues compared to mineral fertilization by 6%, 7% and 6%, respectively. The trend was reversed for all genotypes under WS and under low soil P availability, Lata 3 and Grinkan had a significant FTWF increase of 16% and 19% in the organic N treatment, compared to the mineral N fertilization.

Grinkan had a trend towards lowest T_n under high P at both water levels compared to the other genotypes, while this trend diminishes under low P (Fig. 5). Lata 3 had the trend of having highest T_n values under high P levels in those cylinders with cowpea pre-crop cultivation compared to the other genotypes. The T_n of the other genotypes ranges within the levels of Lata 3 and Grinkan, except for CSV14R in the low P, WS, mineral N treatment with very high T_n values.

3.4 Phenological development and resource acquisition

At stem elongation the plants grown under low P levels had on average over all genotypes approx. 39% lower shoot P content than under high P levels (Table 2). Apart from that, the root to shoot ratios were not significantly different between the P levels, although the early maturing genotypes showed a higher trend of the root to shoot ratios as well as the mycorrhizal infection rates (Table 2). Furthermore, high and positive correlation coefficients at stem elongation shown in the correlation plot (Fig. 7a) illustrate the positive interaction of above and belowground sorghum traits such as shoot biomass, root biomass, root length (Rlength), root surface area (SurfArea) as well as with the transpiration.

Early and late maturing genotypes had contrasting patterns in biomass partitioning among the plant organs. All genotypes had increasing root to shoot ratio with ongoing plant development until flowering, which decreased afterwards for the early maturing genotypes, whereas it remained constant for the late maturing genotypes (Table 2). Throughout the sorghum plant development, the shoot P contents significantly decreased from stem elongation to maturity under both P and water levels (Table 2). However, at maturity shoot P contents were higher under WS compared to WW conditions (Table 2). Such higher shoot P contents resulted later in negative correlations with grain P content (r = -0.49, p = 0.027) and yield (r = -0.51, p = 0.021) (Fig. 7c). The correlation of shoot P with grain P and yield showed similar negative trends. Furthermore, the results display that at maturity high C/N ratios of all plant parts and the transpiration rate were positively correlated with yield formation. Regarding the plant water consumption, the PCA-Biplot (Fig. 7d) demonstrates a negative interaction between the FTWF with yield formation, grain and shoot C/N ratios, as well as grain P and N contents. Furthermore, the clearly distinguishable clustering of the individual treatments within the PCA analysis showed a significant effect of the selected treatments on a multitude of variables of sorghum ecophysiology, which were best explained by the combination of water availability and genotype grouping, resulting in the combinations: early maturing well-watered, early maturing water shortage, late maturing well-watered and late maturing water shortage. The results of the PCA showed significant cluster separation of the late maturing genotypes well-watered cluster to the early and late maturing genotypes under water shortage. The early maturing genotype under well-watered conditions was also significantly different from the late well-watered cluster, while both early maturing clusters (well-watered and water stressed) showed overlaps.

4.1 P limitation for sorghum growth and P mobilization strategies

The reported thresholds for sorghum P deficiency are dependent on the plant development stage during the life cycle. While at early plant stages (23–39 DAS) P concentrations in plant tissues below 2.6 mg g^− 1 can lead to decreased yield (Lockman, 1972), at maturity lower P concentrations around 0.42 mg g^− 1 were reported (Leiser et al., 2012). The results of our study indicate that sorghum grown in low P soil experienced a high P deficiency at early growth stages with P concentrations recorded at 2.01 mg g^− 1. As the plants approached maturity only a moderate P limitation was observed with P concentrations recorded at 0.51 mg g^− 1 (Table 2). However, yield was not negatively affected by the soil P level as long as water supply was sufficient, but shoot biomass was (Fig. 1 and Fig. 2). These results indicate that sorghum has specific characteristic attributes to compensate P limitations which are related to an improved uptake with increasing plant development but also a partitioning strategy that aims for avoiding yield decreases (Leiser et al., 2015). Especially sorghum genotypes originated from West Africa, where soils are characterized as highly P deficient, exhibit a greater efficiency in P uptake and utilization compared to genotypes from a different origin (Seetharama et al., 1984). However, breeding efford can indeed lead to sorghum varieties with improved P use efficiencies (Seetharama et al., 1984).

In fact, improving nutrient and P acquisition dynamics of plants can be achieved through various strategies. One example is the symbiosis with AMF, which can highly improve P uptake at a relatively low soil P availability (P-scavenging strategy). However, at very low soil P concentrations, P-mining strategies with an active increase of P solubility by the release of organic acids were more effective than mycorrhization (Lambers, 2022). In our study, the contribution of AMF nutrient acquisition changed with time and P supply. At anthesis, and only under low P, there was a significant and positive correlation between the shoot P content and degree of AMF infection of roots for the early and late maturing genotypes. Furthermore, the early maturing genotypes from West Africa showed a significant increase in AMF infection at low compared to high P levels (Table 2). The results indicate that the random AMF infection rates alone might not be an appropriate proxy to estimate nutrient supply to the host plant, but would need to be cross validated with the use of isotope tracers (Munene et al., 2024) or reference treatments with soil sterilization. Reason for that is the dynamic and regulated process that equally allows the plant and AMF to actively influence the nutritional exchange (Kiers et al., 2011). Apart from mycorrhization, low P availability might have induced different P mobilizing processes such as carboxylate release (Lambers, 2022) and an increased phosphatase activity (Olander and Vitousek, 2000), so that soil P availability and P uptake might have been increased, although infection rates were similar.

Under P deficiency, plants change their carbon partitioning characteristics and increase their root to shoot ratio (Cakmak et al., 1994; Postma et al., 2014), which was the case for the early maturing genotypes at stem elongation and maturity (Supplement, Table 7), while at anthesis root to shoot ratio was high at both P levels. The late maturing genotypes showed only a trend of a higher root to shoot ratio at maturity and other measured root parameters were similar between the P levels. This suggests that genetic adaptation of the early-maturing genotypes to the nutrient-poor soils of sub-Saharan Africa, leads to increased root-to-shoot ratios to cover the high nutrient demand at flowering.

A major consequence of P limitation is a prolonged plant development of all sorghum genotypes including delayed flowering (Fig. 6) as reported similarly under field conditions (Leiser et al., 2012). Organic residues seemed to enhance the P availability under low P as the flowering time point was significantly reduced, while the organic residues had no influence on the flowering time point in the high P soil. Several studies, revealed that cowpea mobilized P from non-labile sources and increased the P cycling (Krasilnikoff et al., 2003; Pypers et al., 2006), so that P was accessible to the following crop (Alvey et al., 2001). Field experiments with legume-cereal crop rotations described an increased cereal (maize and sorghum) biomass and yield production in the crop rotation compared to the continuous cereal cropping(Sauerborn et al., 2000;Alvey et al., 2001; Franke et al., 2018). In this study only a biomass increase could be confirmed after legume cropping (Fig. 1) and there was only a positive trend for a yield increase (Fig. 2). However, besides mere productivity also fertilizer costs are a major factor affecting the farmers revenues, which can be increased by legume-cereal rotations reducing fertilizer consumption (Tonitto and Ricker-Gilbert, 2016). In any case, this study demonstrated that sorghum genotypes could maintain yield production under low P soil contents due to their P mobilizing strategies. We could not prove increasing P uptake by soil exploitation strategies linked to larger root systems (Parra-Londono et al., 2018), which mighed have been an artefact of the experimental set-up. Most probably, P mobilization processes linked to the AMF symbiosis which was enhanced at essential time points of plant development were the main belowground strategies for the plant P supply, while a high plasticity of the root-to-shoot ratio was a key trait which maintained P supply to the sink organs within the plant and sustained yield production under low P soil levels.

4.2 Key traits to overcome water limitations

Drought is a major constrain for crop yield production. Although sorghum is considered as a drought adapted crop, there is a large genetic variability (Reddy et al., 2008b). Considering yield production, the early maturing genotypes exhibited superior performance compared to the late maturing ones, although the yield of all genotypes was significantly decreased by water shortage (Fig. 2). The results indicate that the early flowering of the genotypes Lata 3 and Grinkan resulted in the advantage of higher amounts of remaining water after flowering compared to the late maturing genotypes. The observation is in accordance with other studies with drought adapted sorghum genotypes displaying an early developmen and smaller plant size (Borrell et al., 2014). The optimal distribution of transpiration is crucial for yield maximization with a threshold of 30% amount of water transpired after flowering optimizing capacities for a high yield production (Ahmed et al., 2018; Passioura and Angus, 2010). This matches the results of our study, where the amount of transpiration after flowering averaged 25–47% (Fig. 4) for the early maturing genotypes Lata 3 and Grinkan, which had the highest yield production under drought. The late maturing genotypes had < 20% of the available water left for transpiration after flowering and thus, had almost no yield production. Harvest index increased from 0.1 with 10% water used up to 0.45 with 20–30% water used after anthesis by the early maturing genotypes and a low FTWF was positively correlated with higher yields (Fig. 7d). However, the processes underlying the water conservation differed in morphological and physiological adaptations between the early maturing genotypes. Lata 3 maintained a relative high transpiration rate per unit leaf area which was caused mainly by a lower LA and leaf senescence (Supplement: Fig. 1 LA), also confirmed in other studies (Blum and Arkin, 1984). Grinkan exhibits characteristics of water conserving traits even under well-watered conditions, as T_n is reduced compared to the other genotypes in most of the treatment combinations (Fig. 5). An explanation might be the increasing root to shoot ratio evolving first during stem elongation and elaborating until flowering, which leads, on the one hand, to an increased water availability of the roots and consequently to a higher root water influx (Bacher et al., 2022). In contrast, drought adaptation by lowering the transpiration per leaf area would lead to a lower photosynthetic activity and cropping would be suitable in environments with low but frequent precipitation events (Turner and Nicolas, 1998; Vadez et al., 2011). Altered physiological changes in aboveground plant organs in response to drought stress are often linked to an altered carbon investment in belowground traits (Freschet et al., 2018), which was confirmed in our dataset by the relative higher investment in root biomass by the water conserving early maturing varieties (Table 2). A high plasticity in the various water conversation traits of sorghum genotypes might be crucial for yield improvement in water prone environments (Gholipoor et al., 2012). A fast plant development coupled with a higher root to shoot ratio, which increase the potential water uptake compared to the LA are the major traits of the early maturing sorghum genotypes to maintain yield production under drought compared to the late maturing genotypes. The advantage can be even increased with including water saving strategies, as low T_n as it was the case for Grinkan.

4.3 Implications of multiple resource limitations on sorghum

The results revealed that on average sorghum could maintain a good productivity even when grown on P limited soils, however under water shortage shoot and yield was decreased compared to plants grown under well-watered conditions on high P soils. These results demonstrate the strong dependency of plant P supply on P mobilization and diffusion processes in soil, which are mainly controlled by the soil water content (Koester et al., 2021). Due to the high reactivity of P, only a low concentration ranging from 0.6 to 11 µM is available in the soil solution according to Plaxton and Lambers (2015), and the transport of these P ions to the plant is exacerbated under restricted soil water contents, as it is mainly driven by diffusion (Bhadoria et al., 1991).

Comparing the yield of the sorghum genotypes under water stress, the early maturing genotypes had an advantage not exclusively due to their faster development, but particularly due to their water saving traits (Fig. 4). When sorghum cultivation is combined with cowpea pre-cropping, the organic residues in the soil accelerated the plant development by increasing plant available P and possibly other nutrients and thus, the flowering time point decreased even on low P soils in case they contain organic residues (Fig. 6). However, the faster development under low P with organic residues was accompanied with higher transpiration rates prior flowering (Fig. 4), so that under water shortage less than 30% transpiration remained post-flowering causing also a yield reduction (Ahmed et al., 2018; Passioura and Angus, 2010). Thus, the advantage of a faster development was leveled out by a higher pre-flowering transpiration. For implementing sustainable management system, particularly in drought prone areas, the practice of pre-cropping and the choice of the respective pre-crops play a crucial role in ensuring nutrient input into low-fertile soils and an adequate water supply for the main crops (Thorup-Kristensen and Kirkegaard, 2016). The knowledge about the soil rhizosphere interactions as well as the impact of the root morphology on yield production in semi-arid regions may be as relevant (Lynch, 2007), as shown by this study. An increased root to shoot ratio is a plant trait which is of similar importance for P deficiency (Cakmak et al., 1994) as for water shortage (Bacher et al., 2022), for each of the sorghum genotypes studies, irrespective of plant development. Our results also indicate that sorghum genotypes with a higher root to shoot ratio show enhanced water saving traits at anthesis resulting in higher yield production at maturity (Fig. 7b and c).

Tube density was selected to mimic plant density under field conditions. Nevertheless, cultivation in tubes avoids root growth in lateral direction and thus root-root interaction among individuals. However, for this study maybe of higher relevance was the limitation to a soil depth of approx. one meter. Although 1.2 m is pretty deep, highly weathered tropical soils often exceed this soil depth and Sorghum is specifically adapted to such soils, reported to reach rooting depth between 1.5 m (Tsuji et al., 2005) and 1.85 m (Stone et al., 2001). Such deep rooting crops have the advantage in reaching additional water resources and to maintain growth and yield production in stored moisture of deep sub-soils (Lynch, 2007). This might be a trait of the late maturing genotypes with their higher total shoot and root biomass. M35-1 was used very successful in ICRISATS’ breeding programs and has a positive reputation by local farmers (Reddy et al., 2009). Thus, the soil volume, specifically depth, restriction of the tubes could be one explanation why late maturing genotypes might not have been able to develop their full potential for drought resistance in this study.

Sorghum genotypes displayed a high potential for sufficient P mobilization and P uptake under well-watered conditions even on infertile soils (Leiser et al., 2012). Water scarcity, in contrast, severely restricted yield, so that water saving traits and the optimal time point of water consumption were the major features maintaining yield production (Passioura and Angus, 2010). Morphological and physiological changes revealed the close interactions between above and belowground traits and their functions under multiple resource limitations. The best-matching combination for nutrient-poor soils in semi-arid areas with high drought risk seemed to be early-maturing varieties with high root to shoot ratio, rapid AMF establishment and low T_n – in this study realized in the genotype Grinkan. Such genotypes have a relatively robust P uptake withstanding low soil availabilities, save water prior flowering and reduce their post flowering water stress.

Competing Interest

We confirm that none of the authors have any conflicts of interest associated with this publication. Also, we confirm that the manuscript has been read and approved by all authors.

Funding

The experiments were funded by the grants associated to the Robert-Bosch Junior Professorship 2017. The study and the exchange with ICRISAT was partly funded by DAAD (PPP Project Nr. 57390361).

Author contributions

MAD, MAA, JC and RPR conceived and designed the study. SL, EMG, LKE, KS, MAD and AMS acquired the data. SL led data analysis but all authors were involved in analysis and interpretation. SL drafted the manuscripts and all authors contributed equally to the revision of text, figures and tables.

Acknowledgements

We gratefully acknowledge ICRISAT (Hyderabad, India) for the opportunity to use the phenotyping facilities and especially Rheka Baddam for technical support. We appreciate the help of the Centre for Stable Isotope Research and Analysis (KOSI) of the University of Goettingen. Also, we thank a lot the technical support of Karin Schmidt, Pratiksha Acharya, Prashanth Prasanna, Lukas Wagner, Vinay K. R. Challa, Isabel Barsties and Patrick Tantzen.

Data Availability

The datasets of the current study are available from the corresponding author on request.

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Supplement.docx

Timing of water use and phosphorus exploitation strategies are promising key traits of Sorghum to maintain biomass and yield production under resource limitations

Status:

Version 1

Abstract

Aims

Methods

Results

Conclusions

Figures

1 Introduction

2 Materials and Methods

2.1 Soil parameters

2.2 Experimental set up

2.3 Cowpea cultivation and ¹⁵N labeling

2.2 Sorghum cultivation

2.3 Field measurements

2.4 Analysis and calculations

2.5 Statistical Analysis

3 Results

3.1 Sorghum biomass and grain yield

3.2 Utilization of organic and mineral nitrogen sources by sorghum

3.3 Utilization of Water Resources

3.4 Phenological development and resource acquisition

4 Discussion

4.1 P limitation for sorghum growth and P mobilization strategies

4.2 Key traits to overcome water limitations

4.3 Implications of multiple resource limitations on sorghum

Declarations

Competing Interest

Funding

Author contributions

Acknowledgements

Data Availability

References

Supplementary Files

Status:

Version 1

Timing of water use and phosphorus exploitation strategies are promising key traits of Sorghum to maintain biomass and yield production under resource limitations

Status:

Version 1

Abstract

Aims

Methods

Results

Conclusions

Figures

1 Introduction

2 Materials and Methods

2.1 Soil parameters

2.2 Experimental set up

2.3 Cowpea cultivation and 15N labeling

2.2 Sorghum cultivation

2.3 Field measurements

2.4 Analysis and calculations

2.5 Statistical Analysis

3 Results

3.1 Sorghum biomass and grain yield

3.2 Utilization of organic and mineral nitrogen sources by sorghum

3.3 Utilization of Water Resources

3.4 Phenological development and resource acquisition

4 Discussion

4.1 P limitation for sorghum growth and P mobilization strategies

4.2 Key traits to overcome water limitations

4.3 Implications of multiple resource limitations on sorghum

Declarations

Competing Interest

Funding

Author contributions

Acknowledgements

Data Availability

References

Supplementary Files

Status:

Version 1

2.3 Cowpea cultivation and ¹⁵N labeling