Sustainable Phosphorus Summit: Improving Plant P-Use Efficiency for Food Security

Sustainable Phosphorus Summit in Montpellier highlights the necessity of enhancing plant P-use efficiency due to P-deficient soils and environmental concerns. Key traits controlling plant responses to P-deficiency are identified, emphasizing the critical role of phosphorus in agricultural sustainability and food security.

• Sustainable agriculture
• Phosphorus efficiency
• Plant responses
• Food security
• Environmental sustainability

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1. Sustainable Phosphorus Summit, Montpellier Sep 2014 http://www.beobachter.ch/typo3temp/pics/Sahara_Dringras_ce99e203b5.jpg Understanding the genetic control of rhizosheath formation and impacts of multiple stress on phosphorus acquisition http://biology.burke.washington.edu/herbarium/imagecollection/wtu6500-6999/md/wtu006608_md.jpg Tim George Ecological Sciences The James Hutton Istitute

2. Productive agricultural land scarce resource Only 30% of the Earth s surface is land, and only 9% of this land area is cultivated, which will not increase Nearly 33% of the worlds arable land lost to erosion or pollution in the last 40 years. LARGE SCALE PIVOT IRRIGATION SYSTEMS Erosion rates from ploughed fields average 10-100 times greater than rates of soil formation. UPLAND PADDY RICE SYSTEMS LARGE SCALE ARABLE PRODUCTION

3. Food Security Demand for Food Population Growth Balanced Western Diet We need to produce as much food in the next 50 years as we have in the last 10000 with fewer inputs

4. The need to improve the P-use efficiency of plants Many soils are P-deficient - agricultural systems respond significantly to P application Efficiency of P fertilizer use is poor - 10 to 50% recovery of applied P - fixation of P in soil & accumulation of total soil P Environmental problems with P mismanagement - eutrophication of aquatic environments - need to reduce the P-load on a landscape scale Future trends towards P-deficit - Rock-P is a finite resource - Nutritional drought caused by water deficit - agriculture will reach nutrient limited productivity ceilings

5. Key traits identified from regulatory pathways controlling plant response to P-deficiency Decreased Photosynthesis Decreased Shoot Growth Replacement phospholipids Decreased Shoot P Increased Shoot Sucrose Increased Root Sucrose Decreased Root P PHR1 Cascade Pi Transporters Phosphatase Mycorrhizal Symbiosis Organic Acid Efflux Root Hair Production Increased Root Growth Hammond & White 2008 JXB 59:93

6. First account as a peculiar sheath, composed of agglutinated particles of sand critical for tolerance to severe drought Price 1911 New Phytologist 10:328-340 Aristida pungens Sahara, North Africa SEM of Maize Rhizosheath Thinner than most cereal Rhizosheaths Intimate interaction between root hairs and mucilage McCully 1999 Ann Rev Plant Phys Plant Mol Biol 50:695-718

7. Large genotypic variation in rhizosheath formation 250 200 Rhizosheath Weight (g g-1 root) 150 100 50 0 Elite and Mutant Spring Barley Varieties 144 Genotype = 12.1-fold variation (mutants - red) 5.1-fold variation (association population - blue) George et al. New Phytologist 203:195-205

8. Rhizosheath improves growth in sub-optimal P and dry conditions 6 5 Biomass Production (g) 4 P0 3 P250 2 P500 1 0 Small (20 g g-1) Moderate (102 g g-1) Large (197 g g-1) Rhizosheath Size

9. Rhizosheath mapped to chromosome 2 using AMP Putative candidate genes include: calcium/calmodulin-dependent protein kinase (OsCDPK7) glutamate receptor (GLR3.1) QTL s on 2H Drought tolerance Root elongation Root length, Root dry weight -log10fp Chromosomal Position (cM)

10. Relationship between rhizosheath and root hair length in populations Root hair length v Rhizosheath weight Mutant Population 1.0 y = 0.1281x - 0.0103 R2 = 0.8979** 0.8 Root hair length (mm) 0.6 0.4 0.2 Association Population 0.0 70 Rhizosheath Weight g cm-1root 0 2 4 6 60 Rhizosheath weight (g) 50 40 30 20 10 0 0 0.5 1 1.5 2 2.5 3 Root Hair Length George et al. New Phytologist 203:195-205

11. Similar observations in wheat by Delhaize et al. Aluminium Tolerance allele of TaALMT1 Delhaize et al. 2012 New Phytologist 195: 609-619

12. Rhizosheath Phylogeny George et al. (2014) New Phytologist 203:195-205 Poales Asparagales 5-fold geneotypic variation in barley QTL for trait on Chromosome 2H Candidate genes include root growth genes and drought tolerance Rhizosheath is only found in Poales? 42 species across 9 orders screened Asterales

13. Summary The ability of crops to cope with abiotic stress needs to be improved. Plants have a number of ways to improve P acquisition: Root Morphology Organic acids Phosphatases Interaction with microorganisms mycorrhizal symbiosis Root hair formation Root hair presence is key to maintaining yield under stress and root hair length is strongly related to rhizosheath formation in controlled and field conditions. Large genotypic variation and genetic association for rhizosheath formation exists and impacts P acquisition. A putative QTL for rhizosheath has been mapped to chromosome 2- a number of candidate genes present in this region. Rhizosheath is present in a range of groups across the phylogeny so relevant to a range of crops not just cereals. Future crops will benefit from maintenance or enhancement of the rhizosheath trait.

14. Acknowledgements Plant Soil Ecology Sub-Programme Lawrie Brown Philip White Personal Research Fellowship Lionel Dupuy Glyn Bengough Bill Thomas Barley Genetics RESAS Workpackage 3.3 Luke Ramsay Joanne Russell Induced Mutations Grant

16. Root hair mutant phenotypes No Root Hairs (NRH) Short Root Hairs (SRH) Long Root Hairs (LRH) Brown et al. 2012 Annals Botany 110: 319-

17. Rhizosheath reduced in some mutants LRH NRH Rhizosheath weight by genotype 8 P0 P500 LSD p< 0.05 6 Rhizosheath weight (g) 4 2 0 SRH-1 SRH-2 SRH-3 Wild-Type NRH-1 NRH-2 NRH-3 LRH-1 LRH-2 LRH-3 Genotype Brown et al. 2012 Annals Botany 110: 319-

18. Shoot Biomass (mg plant-1) 40.8 1100.0 x27 Shoot P Conc (mg P g-1) 0.6 7.5 x13 P accumulation ( g plant-1) 24.2 8200.1 x340 Barley Alfisol 26 days P Added No P

19. In-vitro mutant screen for root phenotype Analyse mutants with desired phenotype (size, root length, root hairs) to elucidate genetic basis for the trait basis for the trait Analyse mutants with desired phenotype (size, root length, root hairs) to elucidate genetic Screen SCRI Optic barley mutant population (9000 -22000 individuals) under controlled conditions of low P and a range of water contents No Root Hairs Short Root Hairs Long Root Hairs

20. In-vitro mutant screen for root phenotype 2%2% 1% As Standard = More Root Hairs + Longer Root Hairs + Agravitropic + Slightly Longer Roots + Very Dense Root Hairs + Short Roots - Short Root Hairs - Slightly Shorter Roots - Fewer Root Hairs - Slightly Shorter Root Hairs - Hairless - Very Short Root Hairs - 5% 25% 7% 19% 5% 2% 1% 1% 0% 30% 458 Mutant Lines

21. Root hair length reduced in some mutants P0 1.6 a P500 1.4 b 1.2 bc Root hair length (mm) c bc 1 d 0.8 0.6 e e 0.4 0.2 f f 0 NRH SRH LRH WT P Phenotypes

22. Absence of root hairs limits P-deficient yield 120 % Relative effectiveness of phenotype on yield 100 LSD (p,0.05) 80 60 40 20 0 NRH SRH LRH WT Phenotype

23. Rhizosheath trait mapped to chromosome 2 Significant Association Chromosome 2 -log10fp Map Distance cM

24. Wheat Rhizosheath picture M. Watt Rhizosheath only found in Poales which include all cereals BUT some suggestion may exist in other orders Duell & Peacock 1985 Crop Science 25:880-883

25. Presence of root hairs enhances rhizosheath in the field

26. Similar variation in chromosome substitution lines

27. Presence of rhizosheath allows tolerance to extreme combined stress Rhizosheath Size Moderate Small SRH Large NRH LRH Relative shoot biomass Relative Shoot Biomass (wrt optimal P) Relative Shoot Biomass (wrt optimal P) 100 Relative Shoot Biomass (wrt optimal P) 100 100 0 20 40 60 80 100 80 80 80 60 60 60 40 500 40 P added ( g P mg-1) 400 20 500 40 P added ( g P mg-1) 300 400 20 500 0 P added ( g P mg-1) 200 300 400 20 90 0 80 100 300 200 70 90 % Field Capacity 0 60 80 200 0 100 50 70 90 % Field Capacity 60 80 100 0 70 50 % Field Capacity 60 0 50 Microarray analysis done under drought conditions in contrasting genotypes

28. Genotypes with no rhizosheath have a different transcriptional response 248 genes differentially regulated under extreme combined P and water stress specific to genotypes without rhizosheath Differential regulation of putative PUE and rooting habit genes Others include genes involved in: P-deficit response biological stress tolerance water-stress tolerance oxidative stress tip growth membrane restructuring