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Plant mineral nutrition from young
 to old soils




Etienne Laliberté and Hans Lambers
School of Plant Biology
The University of Western Australia
www.elaliberte.info
BCI, January 10, 2013
Soil P during pedogenesis
                 Apatite
                 (phosphate minerals)




Mineral P




                                                   Total P

     Organic P

                    Soil age
                                        Walker & Syers (1976) Geoderma
P-poor soils in southwestern Australia




       <0.02% or
       <200 mg kg-1




 http://www.anra.gov.au/topics/soils/pubs/national/agriculture_asris_phos.html
Leaf [P] very low in SW Australia




                     Lambers et al. (2011) Plant Physiol
N/P ratios of mature leaves
                     Westman     Rundel/       Wright et al./   Han et al.   Grigg et al.
Region               & Rogers   Diehl et al.   Niinimets et
                                                    al.

Australia            23.1        24.2            25.8/                         26.6
                                                 31.2
SW Australia                     24.2            24.2
California, USA                  10.8                 N/P ratios >20: P limited;
Chile                            9.2/                 N/P ratios <10: N limited
                                 12.1
France                           14.9
Greece                           15.7
S. Africa (fynbos)               26.4            22.9
China                                                            14.4
“World”                          17.6            18.2


                                                          Lambers et al. (2010) Plant Soil
25                                                                                                      c     (a )

                                                                                                                                                                            Amax expressed per leaf
               s )
 -1



                                                                                   bc
                                                            abc                                                      ab        abc
 -2




                                              20                                                                                           ab
               A m a x ( m o le C O m



                                                                         ab                     a         a

                                                                                                                                                                              area, mass and [P]
                                          2




                                              15

                                              10

                                                5

                                                0



                                              100
     s )
-1




                                                                                                                                                            (b )
                                                                                   d
                                                                                                                     cd                    cd
-1




                                               80
     A m a x (n m o le C O g




                                                                                                                                                     b cd
                                                            b cd
                            2




                                                                                                                               bc
                                               60                        ab                  ab
                                                                                                          a
                                               40


                                               20


                                                0
        s )
-1




                                              0 .6
-1
        A m a x (m m o le C O [g le a f P ]




                                                                                                                                            e               (c )
                                                                                                                     d
                                              0 .4                                                      cd
                                                                                   cd       a b cd                             b cd
                                   2




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                                                                                                                                .l
                                                                                   .b


                                                                                             ae


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                                                                                                                     B
                                                            .m




                                                                                                                                           .s




                                                                                                                                                                   Denton, M.D., Veneklaas, E.J., Freimoser, F.M. & Lambers,
                                                                     .p
                                                .a




                                                                                                                               B
                                                                                 B


                                                                                            m

                                                                                                     .h




                                                                                                                                       B
                                                                     B
                                                           B
                                               B




                                                                                        ha


                                                                                                    B
                                                                                       .c




                                                                                                                                                                   H. 2007. Plant Cell Environ. 30: 1557-1565.
                                                                                   B
Habitats of plants measured in Lesueur
                           National Park




Photos: Marion Cambridge
We measured [P] and
     photosynthesis of young
      expanding leaves, and
         mature leaves


                                   Banksia attenuata
                           young




      Hakea neurophylla

Photos: Marion Cambridge
Rates of photosynthesis of mature leaves are
quite high; those of expanding leaves are not




                                   Lambers et al (2012) New
                                   Phytol
Leaf [P] in Proteaceae declines sharply when
                           leaves mature




Lambers, H., Cawthray, G.R., Giavalisco, P., , Juo, J., Laliberté, E., Pearse, S.J., Scheible, W.-R., Stitt, M. Teste, F.
& Turner, B.L. 2012. New Phytol.
Where might mature leaves of P-efficient
                   Proteaceae economise?




Lambers, H., Finnegan, P.M., Laliberté, E., Pearse, S.J., Ryan, M.H., Shane, M.W., & Veneklaas, E.J.. 2011.
Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: are there lessons for
future crops? Plant Physiol. 156: 1058-1066.
All six Proteaceae species showed a shift from P-
          lipids to other lipids when leaves matured




Lambers, H., Cawthray, G.R., Giavalisco, P., Kuo, J., Laliberté, E., Pearse, S.J., Scheible, W.-R., Stitt, M. Teste, F.
& Turner, B.L. 2012. Proteaceae from severely phosphorus-impoverished soils replace phospholipids by
galactolipids and sulfolipids to achieve a high photosynthetic phosphorus-use efficiency. In prep.
What special features allow the non-
  mycorrhizal plants in Western
Australia to acquire nutrients from
          very poor soils?




Many have cluster roots, as illustrated here
Proportions of species with different nutrient-acquisition strategies




            All plants                             All Western Australian Plants


          Orc
                                                        ECM


  NM
                                                   NM


                AM                                                   AM
                                       AM
                                       NM
                                       ECM
                                       Ericoid
                                       Orchid

Brundrett, M.C. 2009. Mycorrhizal associations and other means of nutrition of vascular
    plants: Understanding the global diversity of host plants by resolving conflicting
     information and developing reliable means of diagnosis Plant Soil 320: 37-77.
Developmental aspects of cluster roots




                 0        1-2     4-5       7-8             12-13           20-21
Shane, M.W., Cramer, M.D., Funayama-Noguchi, S., Cawthray, G.R., Millar, A.H., Day, D.A. & Lambers, H.
                                 2004. Plant Physiol. 135: 549-560.
Respiration and carboxylate exudation in
                              cluster roots of Hakea prostrata
                          10


                                   Respiration
                           8
C use (nmol g-1 FW s-1)




                           6


                                                 Carboxylate
                           4                     exudation

                           2



                                                                          Shane et al. 2004.
                           0
                                                                    Plant Physiol. 135: 549-
                               0         10           20       30                       560.
                                         Time (days)
CYTOSOL                    Lambers, H., Chapin, F.S.III & Pons, T.L. 2008. Plant Physiological Ecology, 2nd
                                                                              edition. Springer, New York.
                        carboxylates                                                           Fe2+
          H+                                                Pi
 ATP           ADP+Pi
                                  phosphatases




  H+                               phosphatases                    H+
    H+                                                                                     Fe2+
         H+      carboxylates                       Pi                carboxylates
                                     Po                     Pi
SOIL                                                                            Al-, Ca-, Fe-
                     Al-Po           Al-Pi
                                                                               carboxylates
                   Fe-Po            Fe-Pi
                   Ca-Po               Ca-Pi                                        elution/
                                                                                  precipitation
Long-term soil chronosequences
Franz Josef glacier
New Zealand
Jurien Bay >2-million-year dune   Jurien
                                     Bay
           chronosequence
                                     Perth


0-7 ky


120-500 ky


         >2000 ky
Soil chronosequences as [P] gradients
  Franz Josef, New Zealand           Jurien Bay, SW Australia




  101   102   103    104      105
   Approx. soil age (years)



Richardson et al. (2004) Oecologia
                                          Laliberté et al. (2012) J Ecol
Soil [N] during soil development
      Franz Josef, New Zealand               Jurien Bay, SW Australia




            101   102   103   104      105
            Approx. soil age (years)


                                                   Laliberté et al. (2012) J Ecol
Richardson et al. (2004) Oecologia
Shift from N to P limitation

    Total P
               Total N




              Soil age
Shift from N to P limitation

            Total P
                       Total N
N-limited




                      Soil age
Shift from N to P limitation

             Total P
                        Total N
N-limited




                       Soil age
    N/P co-limited
Shift from N to P limitation

             Total P
                        Total N
N-limited

                                  P-limited



                       Soil age
    N/P co-limited
Nutrient limitation bioassays

        N limitation




         N/P co-limitation



         P limitation


                             Vitousek and Farrington (1997) Biogeochemistry
Nutrient limitation bioassays




Laliberté et al. (2012) J Ecol
Plant nutrient-use efficiency
NUE = carbon fixed per
unit nutrient taken up


Green leaf nutrient concentration



         Leaf lifespan



 Resorption from senescing leaves
 • profiency = concentration
 • efficiency = % of green          Photo: Patrick Hayes
Franz Josef glacier
 Leaf [N] ⇧ then ⇩ with soil
 age



 Leaf [P] ⇧ then ⇩ with soil
 age


 Both N and P resorption efficiency
 ⇧ with soil age

 N resorption efficiency NOT high in
 young soils
                 Richardson et al. (2004) Oecologia
Primary AIM: To assess how leaf [N] and [P] and
resorption were influenced by soil age across a 2-million
year dune chronosequence in southwestern Australia

0-7 ky


120-500 ky


         >2000 ky
Phosphorus-acquisition strategies
                               P ‘scavengers’ = Mycorrhizal fungi   P ‘miners’ = non-mycorrhizal/cluster roots
Read et al. 1985 New Phytol.




                                                                                Lambers et al (2008) Trends Ecol Evol
Nitrogen fixation
        Acacia lasiocarpa, root nodules
        young dunes, Jurien Bay, SW Australia
2nd AIM: To investigate differences in leaf [N] and [P] and
 resorption between contrasting nutrient-acquisition strategies
Ectomycorrhizal                  Arbuscular mycorrhizal          Nitrogen fixing




                  Cluster root                                         Dauciform roots
                                             Sand-binding root
Non-mycorrhizal strategies
        Successful in P-poor soils
        Combine specialised structure and metabolism
        Release large amounts of carboxylates to mobilised sorbed P
        Can also mobilise metals such as Mn




Lambers et al. (2008)
Cluster roots and Mn accumulation
                          Hakea prostrata (Proteaceae)




                 Shane and Lambers (2005) Physiol Plantarum
Manganese accumulation
• 3rd AIM: To assess Mn accumulation across a
  range of contrasting nutrient-acquisition
  strategies

                  Cluster root
                  (Proteaceae)
      Dauciform
      (sedges)




                                 Sand-binding
                                 (monocots)
                                            (Shane et al. 2011)
Hypotheses
1. Leaf [P] ⇩ and resorption ⇧ with soil age
2. Leaf [N] ⇧ then ⇩ and resorption ⇩ with soil
   age
3. NM strategies ⇩ leaf [P] and ⇧ P resorption
4. Mn accumulation ⇧ in NM strategies, but
   only in older, P-limited sites
Students   Graham Zemunik
Patrick Hayes                       PhD student
Honours student                     vegetation surveys
Leaf nutrient analyses
Collaboration
between UWA
and STRI (Ben
Turner)
Stage 1: very young dunes
    (10’s—100 years)




       Laliberté et al. (2012) J Ecol
Stage 2: young dunes
 (100’s-1000’s years)
Stage 3: young dunes
    (~7000 years)
Stage 4: old dunes
 (~120,000 years)
Stage 5: very old dunes
  (>2,000,000 years)
Leaf [P]: nutrient-acquisition strategies




- NM species: lowest leaf [P] regardless of soil age
- Variation between strategies highest in youngest dunes
- All strategies converged on similarly very low leaf [P] in the oldest soils: mean =
229 µg P g-1
-Similar pattern for senesced leaf [P] and resorption efficiency
Leaf P resorption efficiency
Leaf [N]: nutrient-acquisition strategies




- High amount of variation between strategies
-N-fixing and AM species show consistently higher leaf [N]
- little variation with soil age
Leaf [N]
N resorption greater in very young and
               old soils
Mn accumulation




-All of the different NM strategies showed higher leaf [Mn] compared to other
strategies regardless of soil age

- Large amounts of carboxylates into the rhizosphere?
Mn accumulation




-Mn accumulation is highest in NM species compared to other strategies
- Interestingly, leaf [Mn] increased with soil age for all strategies
Summary
• Extreme range of leaf [P]
• Leaf [P] ⇩ with soil age
• Leaf P resorption efficiency and
  proficiency ⇧ with soil age
• AM and NF ⇧ leaf [N]
• Little difference in leaf [N] with soil age
• N resorption highest in very young and
  old soils
• Mn accumulation in NM species and in
  older soils: carboxylate release?
• Ecosystem-level consequences? (e.g. litter
  decomposition)
•   Hans Lambers
                                      •   Patrick Hayes
 Acknowledgements                     •   Graham Zemunik
                                      •   Ben Turner
• Thanks to STRI for the invitation   •   François Teste
                                      •   Stuart Pearse
                                      •   Thomas Costes
                                      •   several field workers...

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Smithsonian BCI talk, Nutrient acquisition and use

  • 1. Plant mineral nutrition from young to old soils Etienne Laliberté and Hans Lambers School of Plant Biology The University of Western Australia www.elaliberte.info BCI, January 10, 2013
  • 2. Soil P during pedogenesis Apatite (phosphate minerals) Mineral P Total P Organic P Soil age Walker & Syers (1976) Geoderma
  • 3. P-poor soils in southwestern Australia <0.02% or <200 mg kg-1 http://www.anra.gov.au/topics/soils/pubs/national/agriculture_asris_phos.html
  • 4. Leaf [P] very low in SW Australia Lambers et al. (2011) Plant Physiol
  • 5. N/P ratios of mature leaves Westman Rundel/ Wright et al./ Han et al. Grigg et al. Region & Rogers Diehl et al. Niinimets et al. Australia 23.1 24.2 25.8/ 26.6 31.2 SW Australia 24.2 24.2 California, USA 10.8 N/P ratios >20: P limited; Chile 9.2/ N/P ratios <10: N limited 12.1 France 14.9 Greece 15.7 S. Africa (fynbos) 26.4 22.9 China 14.4 “World” 17.6 18.2 Lambers et al. (2010) Plant Soil
  • 6. 25 c (a ) Amax expressed per leaf s ) -1 bc abc ab abc -2 20 ab A m a x ( m o le C O m ab a a area, mass and [P] 2 15 10 5 0 100 s ) -1 (b ) d cd cd -1 80 A m a x (n m o le C O g b cd b cd 2 bc 60 ab ab a 40 20 0 s ) -1 0 .6 -1 A m a x (m m o le C O [g le a f P ] e (c ) d 0 .4 cd cd a b cd b cd 2 abc ab a 0 .2 0 .0 i ii s on a a na la a tti es te at at in el de yt r ia ic no nu an zi br ph ar ur en ke .l ca r io tte .l .b ae oo B .m .s Denton, M.D., Veneklaas, E.J., Freimoser, F.M. & Lambers, .p .a B B m .h B B B B ha B .c H. 2007. Plant Cell Environ. 30: 1557-1565. B
  • 7. Habitats of plants measured in Lesueur National Park Photos: Marion Cambridge
  • 8. We measured [P] and photosynthesis of young expanding leaves, and mature leaves Banksia attenuata young Hakea neurophylla Photos: Marion Cambridge
  • 9. Rates of photosynthesis of mature leaves are quite high; those of expanding leaves are not Lambers et al (2012) New Phytol
  • 10. Leaf [P] in Proteaceae declines sharply when leaves mature Lambers, H., Cawthray, G.R., Giavalisco, P., , Juo, J., Laliberté, E., Pearse, S.J., Scheible, W.-R., Stitt, M. Teste, F. & Turner, B.L. 2012. New Phytol.
  • 11. Where might mature leaves of P-efficient Proteaceae economise? Lambers, H., Finnegan, P.M., Laliberté, E., Pearse, S.J., Ryan, M.H., Shane, M.W., & Veneklaas, E.J.. 2011. Phosphorus nutrition of Proteaceae in severely phosphorus-impoverished soils: are there lessons for future crops? Plant Physiol. 156: 1058-1066.
  • 12. All six Proteaceae species showed a shift from P- lipids to other lipids when leaves matured Lambers, H., Cawthray, G.R., Giavalisco, P., Kuo, J., Laliberté, E., Pearse, S.J., Scheible, W.-R., Stitt, M. Teste, F. & Turner, B.L. 2012. Proteaceae from severely phosphorus-impoverished soils replace phospholipids by galactolipids and sulfolipids to achieve a high photosynthetic phosphorus-use efficiency. In prep.
  • 13. What special features allow the non- mycorrhizal plants in Western Australia to acquire nutrients from very poor soils? Many have cluster roots, as illustrated here
  • 14. Proportions of species with different nutrient-acquisition strategies All plants All Western Australian Plants Orc ECM NM NM AM AM AM NM ECM Ericoid Orchid Brundrett, M.C. 2009. Mycorrhizal associations and other means of nutrition of vascular plants: Understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis Plant Soil 320: 37-77.
  • 15. Developmental aspects of cluster roots 0 1-2 4-5 7-8 12-13 20-21 Shane, M.W., Cramer, M.D., Funayama-Noguchi, S., Cawthray, G.R., Millar, A.H., Day, D.A. & Lambers, H. 2004. Plant Physiol. 135: 549-560.
  • 16. Respiration and carboxylate exudation in cluster roots of Hakea prostrata 10 Respiration 8 C use (nmol g-1 FW s-1) 6 Carboxylate 4 exudation 2 Shane et al. 2004. 0 Plant Physiol. 135: 549- 0 10 20 30 560. Time (days)
  • 17. CYTOSOL Lambers, H., Chapin, F.S.III & Pons, T.L. 2008. Plant Physiological Ecology, 2nd edition. Springer, New York. carboxylates Fe2+ H+ Pi ATP ADP+Pi phosphatases H+ phosphatases H+ H+ Fe2+ H+ carboxylates Pi carboxylates Po Pi SOIL Al-, Ca-, Fe- Al-Po Al-Pi carboxylates Fe-Po Fe-Pi Ca-Po Ca-Pi elution/ precipitation
  • 18. Long-term soil chronosequences Franz Josef glacier New Zealand
  • 19. Jurien Bay >2-million-year dune Jurien Bay chronosequence Perth 0-7 ky 120-500 ky >2000 ky
  • 20. Soil chronosequences as [P] gradients Franz Josef, New Zealand Jurien Bay, SW Australia 101 102 103 104 105 Approx. soil age (years) Richardson et al. (2004) Oecologia Laliberté et al. (2012) J Ecol
  • 21. Soil [N] during soil development Franz Josef, New Zealand Jurien Bay, SW Australia 101 102 103 104 105 Approx. soil age (years) Laliberté et al. (2012) J Ecol Richardson et al. (2004) Oecologia
  • 22. Shift from N to P limitation Total P Total N Soil age
  • 23. Shift from N to P limitation Total P Total N N-limited Soil age
  • 24. Shift from N to P limitation Total P Total N N-limited Soil age N/P co-limited
  • 25. Shift from N to P limitation Total P Total N N-limited P-limited Soil age N/P co-limited
  • 26. Nutrient limitation bioassays N limitation N/P co-limitation P limitation Vitousek and Farrington (1997) Biogeochemistry
  • 28. Plant nutrient-use efficiency NUE = carbon fixed per unit nutrient taken up Green leaf nutrient concentration Leaf lifespan Resorption from senescing leaves • profiency = concentration • efficiency = % of green Photo: Patrick Hayes
  • 29. Franz Josef glacier Leaf [N] ⇧ then ⇩ with soil age Leaf [P] ⇧ then ⇩ with soil age Both N and P resorption efficiency ⇧ with soil age N resorption efficiency NOT high in young soils Richardson et al. (2004) Oecologia
  • 30. Primary AIM: To assess how leaf [N] and [P] and resorption were influenced by soil age across a 2-million year dune chronosequence in southwestern Australia 0-7 ky 120-500 ky >2000 ky
  • 31. Phosphorus-acquisition strategies P ‘scavengers’ = Mycorrhizal fungi P ‘miners’ = non-mycorrhizal/cluster roots Read et al. 1985 New Phytol. Lambers et al (2008) Trends Ecol Evol
  • 32. Nitrogen fixation Acacia lasiocarpa, root nodules young dunes, Jurien Bay, SW Australia
  • 33. 2nd AIM: To investigate differences in leaf [N] and [P] and resorption between contrasting nutrient-acquisition strategies Ectomycorrhizal Arbuscular mycorrhizal Nitrogen fixing Cluster root Dauciform roots Sand-binding root
  • 34. Non-mycorrhizal strategies  Successful in P-poor soils  Combine specialised structure and metabolism  Release large amounts of carboxylates to mobilised sorbed P  Can also mobilise metals such as Mn Lambers et al. (2008)
  • 35. Cluster roots and Mn accumulation Hakea prostrata (Proteaceae) Shane and Lambers (2005) Physiol Plantarum
  • 36. Manganese accumulation • 3rd AIM: To assess Mn accumulation across a range of contrasting nutrient-acquisition strategies Cluster root (Proteaceae) Dauciform (sedges) Sand-binding (monocots) (Shane et al. 2011)
  • 37. Hypotheses 1. Leaf [P] ⇩ and resorption ⇧ with soil age 2. Leaf [N] ⇧ then ⇩ and resorption ⇩ with soil age 3. NM strategies ⇩ leaf [P] and ⇧ P resorption 4. Mn accumulation ⇧ in NM strategies, but only in older, P-limited sites
  • 38. Students Graham Zemunik Patrick Hayes PhD student Honours student vegetation surveys Leaf nutrient analyses
  • 40. Stage 1: very young dunes (10’s—100 years) Laliberté et al. (2012) J Ecol
  • 41. Stage 2: young dunes (100’s-1000’s years)
  • 42. Stage 3: young dunes (~7000 years)
  • 43. Stage 4: old dunes (~120,000 years)
  • 44. Stage 5: very old dunes (>2,000,000 years)
  • 45. Leaf [P]: nutrient-acquisition strategies - NM species: lowest leaf [P] regardless of soil age - Variation between strategies highest in youngest dunes - All strategies converged on similarly very low leaf [P] in the oldest soils: mean = 229 µg P g-1 -Similar pattern for senesced leaf [P] and resorption efficiency
  • 46. Leaf P resorption efficiency
  • 47. Leaf [N]: nutrient-acquisition strategies - High amount of variation between strategies -N-fixing and AM species show consistently higher leaf [N] - little variation with soil age
  • 49. N resorption greater in very young and old soils
  • 50. Mn accumulation -All of the different NM strategies showed higher leaf [Mn] compared to other strategies regardless of soil age - Large amounts of carboxylates into the rhizosphere?
  • 51. Mn accumulation -Mn accumulation is highest in NM species compared to other strategies - Interestingly, leaf [Mn] increased with soil age for all strategies
  • 52. Summary • Extreme range of leaf [P] • Leaf [P] ⇩ with soil age • Leaf P resorption efficiency and proficiency ⇧ with soil age • AM and NF ⇧ leaf [N] • Little difference in leaf [N] with soil age • N resorption highest in very young and old soils • Mn accumulation in NM species and in older soils: carboxylate release? • Ecosystem-level consequences? (e.g. litter decomposition)
  • 53. Hans Lambers • Patrick Hayes Acknowledgements • Graham Zemunik • Ben Turner • Thanks to STRI for the invitation • François Teste • Stuart Pearse • Thomas Costes • several field workers...

Notes de l'éditeur

  1. lecturer in plant biologysmall teaching loadi get to choose what i want to teachthe topic of thislecture is essentially the main theme of my current research
  2. causes are pretty clear and are due to nutrient limitationyou start with low nitrogen because that comes from the atmospherehowever you start with all the phosphorus you’ll ever have because phosphorus comes mostly from minerals
  3. you don’t need to go as far as Hawaii to find similar long-term soil age sequencesin fact you’re sitting on one right nowall across the Swan Coastal Plain you find systems of dune that range from very young to very old, around 2 million yearsthis is what I use in my current research
  4. you don’t need to go as far as Hawaii to find similar long-term soil age sequencesin fact you’re sitting on one right nowall across the Swan Coastal Plain you find systems of dune that range from very young to very old, around 2 million yearsthis is what I use in my current research