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Kanbar, A. Phosphorous Bio-Economy. Encyclopedia. Available online: (accessed on 08 December 2023).
Kanbar A. Phosphorous Bio-Economy. Encyclopedia. Available at: Accessed December 08, 2023.
Kanbar, Adnan. "Phosphorous Bio-Economy" Encyclopedia, (accessed December 08, 2023).
Kanbar, A.(2021, November 15). Phosphorous Bio-Economy. In Encyclopedia.
Kanbar, Adnan. "Phosphorous Bio-Economy." Encyclopedia. Web. 15 November, 2021.
Phosphorous Bio-Economy

Phosphorus (P) is an essential macronutrient, playing a role in developmental and metabolic processes in plants including energy supply (ATP), gene expression (nucleotides), and signaling (protein phosphorylation).

sorghum phosphorus Pi starvation roots SbPht1 genes infrared spectra ash

1. Introduction

Phosphorus (P) is an essential macronutrient, playing a role in developmental and metabolic processes in plants including energy supply (ATP), gene expression (nucleotides), and signaling (protein phosphorylation). In many agricultural and natural ecosystems, P is the limiting factor of growth [1]. Plants acquire P as inorganic orthophosphate (Pi) ions, which are usually integrated into large and rather immobile complexes in the soil and are therefore only poorly available for the plant, posing a serious constraint on plant productivity [2]. The main source of phosphate fertilisers is Pi-containing rocks. This practice will presumably deplete the known phosphorous mines in the course of a few decades [3]. Therefore, bio-economic approaches using Pi recycling from plant residues will become more important to safeguard the global P reserves. However, such strategies depend on the ability of crop plants to mobilise phosphorus from insoluble complexes, mainly with Al or Fe (in acidic soils), or to forage the irregularly distributed Pi from alkaline soils [4]. Thus, it is mandatory to establish new crop varieties with improved Pi uptake efficiency, as a prerequisite for P recycling by utilisation of residues after harvesting [5].
Sorghum (Sorghum bicolor L.) is an interesting candidate crop, since it has the ability to grow in Pi-poor soil and allows for Pi recycling from its straw [5][6]. Sorghum is a multi-purpose economically important crop for food, fodder, bio-fuel, and other industrial uses [7]. In arid and semi-arid areas, sorghum, as a C4 photosynthetic plant, shows high performance with excellent biomass production within a comparatively short life span [8]. As an additional contribution to the bio-economical valorisation of sorghum, the residuals from the extraction of sugars (sweet type) or from harvesting the grains (grain type) for the production of biochar or ash were explored [5]. This approach towards P recycling shifts the mechanisms of Pi uptake, transport, and sequestration into focus.
Plant species that are adapted to Pi-depleted soils have evolved a set of local and systemic (long-distance) adaptive responses to exploit otherwise inaccessible phosphates in the soil and enhance Pi uptake and recycling [9]. The local responses involve massive alterations in the root system architecture [10], while the systemic responses include stimulation of Pi transport by increasing the expression of high-affinity Pi transporters [11]. The reorganisation of the root system has been intensively studied for the model plant Arabidopsis thaliana. Here, Pi deficiency inhibits primary root growth while stimulating the formation of lateral roots and root hairs [12][13]. To what extent the inhibition of primary root growth can be generalised is questionable, since even within Arabidopsis, only certain ecotypes, such as Col-0, show this response to Pi depletion stress [13]. However, the general response, that is, to allocate more resources to the roots during Pi deficiency and, thus, to have a longer root system, seems to be very general. This response has also been observed for sorghum [14], maize [15], ssp. japonica rice [16], and an additional 14 species of monocotyledonous and dicotyledonous plants tested in a hydroponic culture system [17]. This root system remodelling allows plants to forage a greater soil volume and, thus, to maximise phosphorus uptake [18].
These local responses in the roots act in concert with systemic responses. Generally, turning on the local response by Pi-starved plants leads to the activation of long-distance signals, in order to absorb, utilise, and transport Pi from either internal or external pools [19]. The major road for Pi uptake in plants is through symplastic transport across the plasma membrane after uptake into the root hairs, which uses Pi/H+ symporters belonging to the phosphate transporter 1 (Pht1) gene family [20]. The Pht1 proteins localise to the plasma membrane and account for the bulk of Pi uptake under different ambient concentrations of Pi [21]. While expression of Pht1 genes occurs mostly in the roots, in response to Pi deficiency, some members are also active in the flowers, leaves, and stems, indicating a role for the translocation of Pi inside the plant [22]. The sorghum genome harbours 11 predicted members of the Pht1 family [11].
A deeper understanding of these transporters might contribute to a sustainable management of the global P reserves, through Pi recycling by utilisation of plant residues or ash in agriculture. Known as the oldest fertilisers in the world, combusted biomass ashes delivering minerals have been used as fertilisers from the first day of human civilisation [23]. The recycling of ashes for agricultural purposes may reduce the usage of commercial fertilisers and has the potential to solve the increasing demand of biomass production and, at the same time, the problem of ash disposal [24]. Herein, the mineral ash composition is decisive for the solubility of P [25]. Sorghum ashes contain P and other nutrients needed for plant nutrition [23].

2. Phosphorus Starvation Enhances Primary Root Elongation and Inhibits Shoot Growth

Changing the root and shoot architecture under Pi starvation helps to improve the ability of a plant to forage Pi and represents one of the earliest phenotyping changes [26]. Therefore, we measured the response of root and shoot growth in Razinieh and Della, grown under normal conditions or under Pi starvation. We observed that Pi depletion enhanced the elongation of the seminal root, and of the root dry weight as well (Figure 1A,C). In contrast, shoot elongation stopped under Pi depletion (Figure 1B). Interestingly, the temporal increment in the stem dry weight, composed of leaves and the shoot axis, increased under Pi depletion (Figure 1E), while that of the leaf dry weight decreased (Figure 1D). Thus, the increment in the dry weight for the shoot axis increased, rather than decreased (this effect was more pronounced in Razinieh over Della). This means that the observed arrest of shoot elongation (Figure 1B) is mainly caused by arrested cell expansion (uptake of water), rather than inhibited cell proliferation. As a consequence of the stimulated root elongation and reduced shoot elongation, the ratio of root to shoot length increased as well. However, the dry weight also partitioned more towards the root because the increase in the stem dry weight in response to Pi depletion did not keep pace with the increase in the root dry weight. Both varieties responded to Pi depletion with a substantial accumulation of anthocyanin (Figure 1F). While the overall pattern was comparable between both genotypes, Della displayed a stronger reaction to Pi starvation, as evident from the primary root growth at day 12 of Pi depletion (267.4% compared to 74.4% in Razinieh). This rapid increase in the primary root length of Della was reflected by a corresponding rise in the root dry weight (190.8% compared to 125.6% in Razinieh). These differences were already manifested at day 6 of Pi depletion (Figure 1A,C). These morphological responses probably contribute to the adaptation to Pi deficiency. The extension of the root system caused by the altered cell expansion and proliferation will increase the surface available for absorption and, thus, for foraging Pi from a more extended area to compensate for Pi deficiency [15]. The stimulation of primary root elongation and root dry weight in both sweet and grain sorghum varieties under hydroponic conditions is consistent with earlier observations in sorghum [14], maize [15], and ssp. japonica rice [16]. The situation in Arabidopsis seems to be different, though [27], which is probably related to the completely different root system (the seminal root of Graminea is later replaced by a homorrhizous system, while the seminal root in dicots persists and develops into an allorrhizous system).
Figure 1. Effect of phosphorus starvation on seedling growth of a grain (Razinieh) and a sweet (Della) sorghum variety. The seeds of two varieties were initially grown in agar with 8% MS for 10 days; after that, the seedlings were transferred to half Hoagland solution for 2 days, followed by full Hoagland solution for 4 days to obtain greater adaptation. Thereafter, the seedlings were subjected to 2 mM NH4H2PO4 (normal condition; +Pi) or zero (phosphorous starvation; −Pi). After that, plant sampling was conducted at 0, 6, and 12 days of Pi starvation for measurement of traits. Data are presented for (A) primary root length (cm), (B) shoot length (cm), (C) root dry weight (mg), (D) leaf dry weight (mg), (E) stem dry weight (mg), and (F) anthocyanin content (mg/g FW). Values are means ± SE. ns: not significant; *, **, *** are significant at 0.05, 0.01, and 0.001, respectively, paired two-tailed Student’s t-test; n = 9.
We observed that the shoots did not elongate under Pi starvation, irrespective of the genotype (Figure 1B). In addition, leaf biomass accumulated more slowly under Pi starvation. This inhibition of leaf growth was more prominent in Della (−31.8% at day 12 versus the control condition) compared to Razinieh (−16.7% at day 12 versus the control condition), on the background that leaf growth was, nonetheless, much slower in Della (Figure 1D). This inhibition of shoot growth at concomitantly increasing root proliferation is consistent with previous observations in rice [28], sorghum [29], and Arabidopsis [12][13]. The biological function might be that resources repartition to the root system, supporting their exploration of the soil for patches of Pi [18].
Anthocyanin over-pigmentation is one of the phenotypic characteristics of plants in response to Pi starvation [30]. Measurements of anthocyanin in the shoots (normalised by fresh weight) showed low levels for both Razinieh and Della under normal Pi conditions, but a remarkable increase under Pi depletion stress (Figure 1F). To account for the differences in leaf biomass, we normalised the anthocyanin content on the shoot fresh weight. We see that the ground level in Della is almost twice that of Razinieh, and Della also accumulated more anthocyanin under Pi depletion stress. However, on a relative scale, the increase in Razinieh was stronger (around 235.4% of the ground level at day 12 of Pi depletion) than in Della (around 126.9% of the ground level at day 12), such that under stress, the two genotypes approached each other with respect to pigmentation. These data are consistent with findings in Arabidopsis, where anthocyanin accumulation in response to Pi depletion does not depend on growth [31]. Although showing a reduction in leaf growth, the sweet variety Della retains anthocyanin accumulation, even at higher levels than Razinieh. This has to be seen on the background of the higher level of sugar in the shoot of Della [32] compared to Razinieh [33][34][35]. Since sugars accumulate under Pi starvation [36], it is straightforward to assume that glycosylation of the phenolic moiety and import to the vacuole are crucial for this pigment response. Moreover, activation of secondary metabolism means that resources have to be relocated and are not available for growth, which is a major reason why adaptation to stress comes with a growth cost [37]. However, beyond this impact as limiting factors, sugars exert regulatory functions, acting as signals and cross-talking with hormonal regulation [38]. In Arabidopsis, sucrose can activate anthocyanin biosynthesis through a sucrose importer, MAPK cascade [39]. This culminates in the induction of the transcription factor MYB57/PAP1 that activates the genes of the anthocyanin pathway [40]. The activation of sugar signaling by Pi starvation is well known [41]. A straightforward working model would explain the more pronounced anthocyanin pigmentation in Della as a consequence of the more pronounced accumulation of sucrose in this sweet sorghum genotype.
In summary, the stimulation of root development (accompanied by an inhibition of shoot development) can also be used in sorghum as a reliable phenotypic marker for the adaptation to Pi starvation stress. In contrast, the accumulation of anthocyanin seems to depend on sugar signaling and represents a stress marker, rather than a marker for stress adaptation. Thus, Razinieh and Della contrast with respect to the adaptive versus the stress-reporting responses to Pi depletion.

3. Lateral Root Formation Is Induced by Phosphate Starvation

Reports on the effect of Pi deficiency are discrepant. Even for the same model (Arabidopsis thaliana), both suppression [13] and enhancement [14] have been reported, and for sorghum [15], primary root growth and the production of lateral roots seem to be stimulated. Transferring the conclusions drawn from the seminal roots of Arabidopsis to sorghum is problematic, since both root systems develop through different mechanisms—the seminal root in Arabidopsis persists to give rise to a more or less allorrhizous system, while in cereals such as sorghum, the seminal root decays later and is replaced by a homorrhizous system. In our experiments, primary root elongation was stimulated by Pi depletion in both varieties studied (Figure 1A and Figure 2A–C), and lateral roots were promoted as well, albeit the amplitude and location differed between the two varieties (Figure 2D,E).
Figure 2. Effect of phosphorus starvation on root system architecture and growth of a grain (Razinieh) and a sweet (Della) sorghum variety. The seeds of two varieties were initially grown in agar with 8% MS for 4 days; after that, the seedlings were transferred to big plates with a wedge containing Hoagland solution and 1.5% phytoagar (pH 5.8) for 6 days. The Pi treatments were 2 mM NH4H2PO4 (normal condition; +Pi) or zero (phosphorous starvation; −Pi). Plant sampling was conducted after 6 days of Pi treatments. Data are presented for (A) root system architecture, (B) primary root and shoot lengths of Razinieh (cm), (C) primary root and shoot lengths of Della (cm), (D) number of lateral roots in basal and apical zones of Razinieh, (E) number of lateral roots in basal and apical zones of Della. Values are means ± SE; ns: not significant; *, ***, **** are significant at 0.05, 0.001, and 0.0001, respectively, paired two-tailed Student’s t-test; n = 9.
Already under control conditions, lateral roots were significantly more abundant in Razinieh as compared to Della, and this difference became accentuated under Pi depletion. In the basal half of the seminal root, the difference in lateral root density was almost 3-fold in Razinieh over Della. Interestingly, the situation was different in the apical half of the seminal root. Here, Pi depletion enhanced lateral roots in Della but was inhibitory in Razinieh. As a result, Razinieh produces a much larger number of lateral roots, confined to the basal half of the seminal root (i.e., close to the soil surface). This is expected to result in a greater exploratory capacity to forage the soil for phosphorous [18].


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Subjects: Plant Sciences
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