Crop Response to Low Phosphorus Bioavailability with a Focus on Tomato

Round 1

Reviewer 1 Report

The text was modified according to the reviewer's comments.

Author Response

Thank you for reviewing this article. Revisions have been made to addresses the reviewer’s comments. Changes are tracked in the document.

1. One of the goals of the review is to discuss the current knowledge we have on tomato crops. Yet, discussion on tomato crops is lacking. Please elaborate on more topics such as what test have been done on tomato so far in regard to PAE? How tomato plants get soil P? What strategies are more favorable?
   • We tried to emphasize tomato more in this version of the review. Information on tomato has been added in the introduction, at the beginning of 3.1 Internal phosphorus sensing, 4.1 Root morphological responses – Root plasticity, 4.2 Exudation of root derived compounds – organic acid exudation, 4.2 Exudation of root derived compounds – phosphatase exudation, and 4.3 microbial symbiosis
2. When methods or techniques can we use today to enhance specific characteristics which facilitate plant P uptake? This should be discussed in more detail.
   • More detail was added to specifically discuss how to enhance P acquisition in sections such as 4.2 Exudation of root derived compounds – proton exudation and rhizosphere acidification, 4.2 Exudation of root derived compounds – organic acid exudation, 4.3 microbial symbiosis, and the conclusions
3. I think that an additional table\figure showing which summarize the various traits adopted by different crop plant (tomato or other close species) in different soil conditions is important in this review. Furthermore, additional data on what had actually been done by researchers to increase plant PAE is desirable, including some quantitative data of the effects of various strategies on P acquisition.
   • Table 2 was added to discuss traits in different soils
   • Data from literature was added to sections including 4.1 root morphological responses – root hair production, 4.2 Exudation of root derived compounds – proton exudation and rhizosphere acidification, 4.2 Exudation of root derived compounds – organic acid exudation, 4.2 Exudation of root derived compounds – phosphatase exudation, and 4.3 Microbial symbiosis
4. I would like to see some discussion on the differet P sorption and bioavailability in soils around the world (acidic tropical soils vs alkaline Mediterranean soils, both are very infertile). Most of the arable soils are in the tropics so this is important!
   • A subsection of part 2 was added to address this point (2.3 Phosphorus bioavailability across different soils)
5. Many important papers are not cited. Please see the thorough review by Hinsinger et al (2001) and the many papers by Hans Lambers (many reviews on soil P and plant traits to get P from the soil). Though these papers mainly look at natural ecosystems they still apply for other plants!
   • Much more current literature was incorporated into this version of the article including the specified Hinsinger review and papers by Hans Lambers
6. L35: I think this range can be also lower then 0.1 %. This is an important point. Can you please elaborate on this in another sentence?
   • This has been changed to, “Optimal plant P concentrations typically range from 0.1 to 0.5%, averaging approximately 0.2% [2]. The critical leaf concentration associated with a 10% reduction in dry matter yield for perennial ryegrass (Lolium perenne) is 0.0021% [4] and for drawf saltwort (Salicornia bigelovii Torr.) is 0.00078% [5]. The critical value for P may decline with age as shown by purple bush bean (Macroptilium atropurpureum Moc. and Sessé ex DC) where the critical concentration decreased from 0.03% at 41 days to 0.01% at 77 days [6]. The range of shoot P content tends to be higher on average for crops inoculated with mycorrhizal fungi (0.3-0.4%) compared to uninfected plants (0.1-0.3%) [7].”
7. L58-60: Irrelevant for P soil cycle. Please remove
   • This has been moved to “2.1 Phosphorus pools and sources” and reworded to say, “Phosphoric acid is another popular inorganic fertilizer source derived from reacting rock phosphate with sulfuric acid.”
8. L60: In the soil…first I would write on the P forms in soil (organic vs inorganic)
   • Organic and inorganic forms are specified
9. L67: It doesn’t have to be solid per se, P can also adsorb or precipitate to create semi-crystalline compounds, which are known to exist in the soil
   • This has been changed to, “A precipitation reaction occurs when a cation and anion interact in aqueous forms to produce a solid or a semi-crystalline structure such as aluminum (Al) or iron (Fe) phosphates [38]. Solution phosphate may precipitate with mineral nutrients such as calcium (Ca) [36]…”
10. L68: Adsoprtion can occur with Ca as well
    • This has been changed to, “Solution phosphate may adsorb onto metal oxides and metal hydroxides.”
11. L68-75: This paragraph is very hard to follow. Please revise and make it simpler. I suggest the use of other references for your explanation of Fe-P reactions, there are many more papers which are more recent and look at this topic in more detail.
    • This section has been revised. Please see the second paragraph of 2.2 Soil Phosphorus Fluxes
12. L91: Give P conc. in ug per g soil or ppm, not in molar.
    • This has been changed to ppm concentration
13. L92: Are you sure these are the right concentrations? This is extremely low! Please check again.
    • This line has been removed and replaced by, “Depending on soil test results (Mehlich 3 soil extraction method), UF IFAS recommended P fertilization as P₂O₅ for tomato production is 120-150 lb/A for low, 100 lb/A for medium, and 0 lb/A for high soil test index [25].”
14. L82-100: The entire paragraph is confusing and should be re-written. I am not sure the details on soil pH and P species are relevant here. Furthermore, it is not how we commonly refer to P species in soils. Also, pH is the factor that controls the P sorption to Ca or Fe\Al minerals and its bioavailability. The actual P species (PO34-, HPO42- and so on) is less relevant.
    • This section has been revised for clarity and combined with another to form “2.1 Phosphorus pools and sources”
15. L132- Unlike N, C and S!
    • This has been changed to, “As opposed to the cycles of other nutrients like nitrogen (N) [22], sulfur (S) [23], and carbon (C) [24], there is no gaseous form of P available for fixation.”
16. L147-L150- There is much more new data on phosphate as a finite resource and its environmental and economic consequences (and eutrophication!). I think this paragraph can be improved. It is very important to stress why increasing PUE is desirable. For example, in the tropics most of the farmer's costs go to P fertilization because of the high sorption capacity of the highly weathered soils.
    • The source from 1981 has been replaced by a source from 2009. This paragraph has been revised. Please see the end of section 2.1 Phosphorus pools and sources
17. L152-155: Define Km
    • This has expanded to, “The constant K_m can help describe the kinetics of phosphate transport across a steep concentration gradient. Numerically, K_m equals the concentration of solute that yields half the maximum rate of transport. Low K_m values indicate high binding attraction of the transported compound to the transport site, whereas high K_m values indicate a lower binding attraction [64].”
18. L151: What about foliar uptake? Foliar P fertilization is widely and is very important in some crop plants!
    • Foliar uptake is now discussed. Please see the first paragraph of 2.1 Phosphorus pools and sources.
19. L291: What about malate and oxalate?
    • This has been changed to, “Roots may also exude organic acids such as citrate, malate, fumarate, or oxalate…”
20. L331-353: What is the bottom line? Root fineness increases PAE but root length and number decreases? It is hard to follow.
    • This section has been revised to be clearer. Please see the section, “Lateral root growth to enhance surface area” under the larger section, “4.1 Root morphological responses”
21. L403-409: I would start this section with the last paragraph where you discuss the soil pH. First say that acidification is important in alkaline soils and not in acidic soils.
    • The structure of this section has been changed accordingly
22. L442: This section is lacking. The effect of root organic exudation is very important in poor P conditions. Please see Hinsinger et al review (2001) on soil bioavailable P and plant P traits. This also apply for the pH part.
    • The section on organic acid exudation has been expanded
23. L465-467: This is not true. There are many reports on alkaline phosphatase and plant P traits.
    • Several articles discussing alkaline phosphatase have been incorporated

Author Response File: Author Response.docx

Reviewer 2 Report

Please see the attached document

Comments for author File: Comments.docx

Author Response

Thank you for reviewing this article. Revisions have been made to addresses the reviewer’s comments. Changes are tracked in the document.

One of the goals of the review is to discuss the current knowledge we have on tomato crops. Yet, discussion on tomato crops is lacking. Please elaborate on more topics such as what test have been done on tomato so far in regard to PAE? How tomato plants get soil P? What strategies are more favorable?

1. • We tried to emphasize tomato more in this version of the review. Information on tomato has been added in the introduction, at the beginning of 3.1 Internal phosphorus sensing, 4.1 Root morphological responses – Root plasticity, 4.2 Exudation of root derived compounds – organic acid exudation, 4.2 Exudation of root derived compounds – phosphatase exudation, and 4.3 microbial symbiosis
2. When methods or techniques can we use today to enhance specific characteristics which facilitate plant P uptake? This should be discussed in more detail.
   • More detail was added to specifically discuss how to enhance P acquisition in sections such as 4.2 Exudation of root derived compounds – proton exudation and rhizosphere acidification, 4.2 Exudation of root derived compounds – organic acid exudation, 4.3 microbial symbiosis, and the conclusions
3. I think that an additional table\figure showing which summarize the various traits adopted by different crop plant (tomato or other close species) in different soil conditions is important in this review. Furthermore, additional data on what had actually been done by researchers to increase plant PAE is desirable, including some quantitative data of the effects of various strategies on P acquisition.
   • Table 2 was added to discuss traits in different soils
   • Data from literature was added to sections including 4.1 root morphological responses – root hair production, 4.2 Exudation of root derived compounds – proton exudation and rhizosphere acidification, 4.2 Exudation of root derived compounds – organic acid exudation, 4.2 Exudation of root derived compounds – phosphatase exudation, and 4.3 Microbial symbiosis
4. I would like to see some discussion on the differet P sorption and bioavailability in soils around the world (acidic tropical soils vs alkaline Mediterranean soils, both are very infertile). Most of the arable soils are in the tropics so this is important!
   • A subsection of part 2 was added to address this point (2.3 Phosphorus bioavailability across different soils)
5. Many important papers are not cited. Please see the thorough review by Hinsinger et al (2001) and the many papers by Hans Lambers (many reviews on soil P and plant traits to get P from the soil). Though these papers mainly look at natural ecosystems they still apply for other plants!
   • Much more current literature was incorporated into this version of the article including the specified Hinsinger review and papers by Hans Lambers
6. L35: I think this range can be also lower then 0.1 %. This is an important point. Can you please elaborate on this in another sentence?
   • This has been changed to, “Optimal plant P concentrations typically range from 0.1 to 0.5%, averaging approximately 0.2% [2]. The critical leaf concentration associated with a 10% reduction in dry matter yield for perennial ryegrass (Lolium perenne) is 0.0021% [4] and for drawf saltwort (Salicornia bigelovii Torr.) is 0.00078% [5]. The critical value for P may decline with age as shown by purple bush bean (Macroptilium atropurpureum Moc. and Sessé ex DC) where the critical concentration decreased from 0.03% at 41 days to 0.01% at 77 days [6]. The range of shoot P content tends to be higher on average for crops inoculated with mycorrhizal fungi (0.3-0.4%) compared to uninfected plants (0.1-0.3%) [7].”
7. L58-60: Irrelevant for P soil cycle. Please remove
   • This has been moved to “2.1 Phosphorus pools and sources” and reworded to say, “Phosphoric acid is another popular inorganic fertilizer source derived from reacting rock phosphate with sulfuric acid.”
8. L60: In the soil…first I would write on the P forms in soil (organic vs inorganic)
   • Organic and inorganic forms are specified
9. L67: It doesn’t have to be solid per se, P can also adsorb or precipitate to create semi-crystalline compounds, which are known to exist in the soil
   • This has been changed to, “A precipitation reaction occurs when a cation and anion interact in aqueous forms to produce a solid or a semi-crystalline structure such as aluminum (Al) or iron (Fe) phosphates [38]. Solution phosphate may precipitate with mineral nutrients such as calcium (Ca) [36]…”
10. L68: Adsoprtion can occur with Ca as well
    • This has been changed to, “Solution phosphate may adsorb onto metal oxides and metal hydroxides.”
11. L68-75: This paragraph is very hard to follow. Please revise and make it simpler. I suggest the use of other references for your explanation of Fe-P reactions, there are many more papers which are more recent and look at this topic in more detail.
    • This section has been revised. Please see the second paragraph of 2.2 Soil Phosphorus Fluxes
12. L91: Give P conc. in ug per g soil or ppm, not in molar.
    • This has been changed to ppm concentration
13. L92: Are you sure these are the right concentrations? This is extremely low! Please check again.
    • This line has been removed and replaced by, “Depending on soil test results (Mehlich 3 soil extraction method), UF IFAS recommended P fertilization as P₂O₅ for tomato production is 120-150 lb/A for low, 100 lb/A for medium, and 0 lb/A for high soil test index [25].”
14. L82-100: The entire paragraph is confusing and should be re-written. I am not sure the details on soil pH and P species are relevant here. Furthermore, it is not how we commonly refer to P species in soils. Also, pH is the factor that controls the P sorption to Ca or Fe\Al minerals and its bioavailability. The actual P species (PO34-, HPO42- and so on) is less relevant.
    • This section has been revised for clarity and combined with another to form “2.1 Phosphorus pools and sources”
15. L132- Unlike N, C and S!
    • This has been changed to, “As opposed to the cycles of other nutrients like nitrogen (N) [22], sulfur (S) [23], and carbon (C) [24], there is no gaseous form of P available for fixation.”
16. L147-L150- There is much more new data on phosphate as a finite resource and its environmental and economic consequences (and eutrophication!). I think this paragraph can be improved. It is very important to stress why increasing PUE is desirable. For example, in the tropics most of the farmer's costs go to P fertilization because of the high sorption capacity of the highly weathered soils.
    • The source from 1981 has been replaced by a source from 2009. This paragraph has been revised. Please see the end of section 2.1 Phosphorus pools and sources
17. L152-155: Define Km
    • This has expanded to, “The constant K_m can help describe the kinetics of phosphate transport across a steep concentration gradient. Numerically, K_m equals the concentration of solute that yields half the maximum rate of transport. Low K_m values indicate high binding attraction of the transported compound to the transport site, whereas high K_m values indicate a lower binding attraction [64].”
18. L151: What about foliar uptake? Foliar P fertilization is widely and is very important in some crop plants!
    • Foliar uptake is now discussed. Please see the first paragraph of 2.1 Phosphorus pools and sources.
19. L291: What about malate and oxalate?
    • This has been changed to, “Roots may also exude organic acids such as citrate, malate, fumarate, or oxalate…”
20. L331-353: What is the bottom line? Root fineness increases PAE but root length and number decreases? It is hard to follow.
    • This section has been revised to be clearer. Please see the section, “Lateral root growth to enhance surface area” under the larger section, “4.1 Root morphological responses”
21. L403-409: I would start this section with the last paragraph where you discuss the soil pH. First say that acidification is important in alkaline soils and not in acidic soils.
    • The structure of this section has been changed accordingly
22. L442: This section is lacking. The effect of root organic exudation is very important in poor P conditions. Please see Hinsinger et al review (2001) on soil bioavailable P and plant P traits. This also apply for the pH part.
    • The section on organic acid exudation has been expanded
23. L465-467: This is not true. There are many reports on alkaline phosphatase and plant P traits.
    • Several articles discussing alkaline phosphatase have been incorporated

Author Response File: Author Response.docx

This manuscript is a resubmission of an earlier submission. The following is a list of the peer review reports and author responses from that submission.

Round 1

Reviewer 1 Report

This review discusses the importance of phosphate, one of the essential elements in plant nutrition, in crops, with a focus on Solanum lycopersicum.
Topics of interest linking phosphorus and plants are found throughout the manuscript.
Nevertheless, a large majority of references are old (a little more than 44 are from before the 2000s, and many are from before 2010). Phosphorus is nevertheless a widely studied element. More recent references should be included in the manuscript.
Although the review sweeps over a wide range of points, it is still too general: I recommend that the authors should provide more details in certain paragraphs such as 2.3. and perhaps insist on the relations with other chemical elements.  

Reviewer 2 Report

The manuscript describes the crop response to reduced phosphorus bioavailability with a focus on tomato.

The text is very well-written. Minor points are raised below.

1. References should appear consecutively starting from no 1.
2. 2, l. 56: “Chelation is a process of ligand exchange.” Is this correct? Please, change.
3. 2, ls. 62-65: “In an adsorption reaction, the predominantly positive charge of a mineral edge attracts P anions. Aluminum, iron, and hydrogen-oxide minerals are the main constituents of P adsorption reactions.” Please, explain (which adsorption reactions/mineral edges are meant) providing suitable references.
4. 2, ls. 70-71: “Phosphorous acid (also known as phosphite, phosphonate) (H3PO3 3-) (Phi) forms when a P bound oxygen in orthophosphate is replaced by hydrogen [130].” Is this correct? Please, change.
5. Section 2.1 and 2.3: Which P-containing compound is more beneficial to plants?
6. Fonts should be of equal size throughout the text.
7. “…(divalent cations on CEC increase P adsorption greater than monovalent cations),…”. Please, explain.
8. 3, ls. 105-116: In which sorbent/adsorbate systems are these two equations applied?
9. Section 4.2.2: L. 418: “Organic acids (OAs) complex with metal cations and displace anions from the soil matrix [56].” Please, specify OAs/metal cations/anions.
10. For which element(s) reduced bioavailability, is the crop response similar with that of phosphorus?