Developing naturally stress-resistant crops for a sustainable agriculture

Abstract

A major problem facing humanity is that our numbers are growing but the availability of land and fresh water for agriculture is not. This problem is being exacerbated by climate change-induced increases in drought, and other abiotic stresses. Stress-resistant crops are needed to ensure yield stability under stress conditions and to minimize the environmental impacts of crop production. Evolution has created thousands of species of naturally stress-resistant plants (NSRPs), some of which have already been subjected to human domestication and are considered minor crops. Broader cultivation of these minor crops will diversify plant agriculture and the human diet, and will therefore help improve global food security and human health. More research should be directed toward understanding and utilizing NSRPs. Technologies are now available that will enable researchers to rapidly improve the genetics of NSRPs, with the goal of increasing NSRP productivity while retaining NSRP stress resistance and nutritional value.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: The rapid domestication of NSRPs using precise gene editing.

References

  1. 1.

    Foley, J. A. et al. Solutions for a cultivated planet. Nature 478, 337–342 (2011).

    CAS  Google Scholar 

  2. 2.

    Godfray, H. C. et al. Food security: the challenge of feeding 9 billion people. Science 327, 812–818 (2010).

    CAS  Google Scholar 

  3. 3.

    Shinozaki, K., Uemura, M., Bailey-Serres, J., Bray, E. A. & Weretilnyk, E. in Biochemistry and Molecular Biology of Plants (eds Buchanan, B. B., Gruissem, W. & Jones, R. L.) Ch. 22, 1051–1100 (Wiley, Chichester, 2015).

  4. 4.

    Cai, W. J. et al. Increasing frequency of extreme El Nino events due to greenhouse warming. Nat. Clim. Change 4, 111–116 (2014).

    CAS  Google Scholar 

  5. 5.

    Dai, A. G. Increasing drought under global warming in observations and models. Nat. Clim. Change 3, 52–58 (2013).

    Google Scholar 

  6. 6.

    Battisti, D. S. & Naylor, R. L. Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323, 240–244 (2009).

    CAS  Google Scholar 

  7. 7.

    Pingali, P. L. Green revolution: impacts, limits, and the path ahead. Proc. Natl Acad. Sci. USA 109, 12302–12308 (2012).

    CAS  Google Scholar 

  8. 8.

    FAOSTAT (FAO, 2017); http://www.fao.org/faostat/en/#data/QC

  9. 9.

    Ray, D. K., Ramankutty, N., Mueller, N. D., West, P. C. & Foley, J. A. Recent patterns of crop yield growth and stagnation. Nat. Commun. 3, 1293 (2012).

    Google Scholar 

  10. 10.

    Alston, J. M., Beddow, J. M. & Pardey, P. G. Agricultural research, productivity, and food prices in the long run. Science 325, 1209–1210 (2009).

    CAS  Google Scholar 

  11. 11.

    Lobell, D. B. et al. Greater sensitivity to drought accompanies maize yield increase in the U. S. Midwest. Science 344, 516–519 (2014).

    CAS  Google Scholar 

  12. 12.

    Li, H., Rasheed, A., Hickey, L. T. & He, Z. Fast-forwarding genetic gain. Trends Plant Sci. 23, 184–186 (2018).

    CAS  Google Scholar 

  13. 13.

    Zhu, Y. et al. Genetic diversity and disease control in rice. Nature 406, 718–722 (2000).

    CAS  Google Scholar 

  14. 14.

    Gilliham, M., Able, J. A. & Roy, S. J. Translating knowledge about abiotic stress tolerance to breeding programmes. Plant J. 90, 898–917 (2017).

    CAS  Google Scholar 

  15. 15.

    Zheng, P. et al. A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat. Genet. 40, 367–372 (2008).

    CAS  Google Scholar 

  16. 16.

    Dwivedi, S. L. et al. Landrace germplasm for improving yield and abiotic stress adaptation. Trends Plant Sci. 21, 31–42 (2016).

    CAS  Google Scholar 

  17. 17.

    Munns, R. et al. Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat. Biotechnol. 30, 360–364 (2012).

    CAS  Google Scholar 

  18. 18.

    Tardieu, F. Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. J. Exp. Bot. 63, 25–31 (2012).

    CAS  Google Scholar 

  19. 19.

    Mittler, R. & Blumwald, E. Genetic engineering for modern agriculture: challenges and perspectives. Annu. Rev. Plant Biol. 61, 443–462 (2010).

    CAS  Google Scholar 

  20. 20.

    Cooper, M., van Eeuwijk, F. A., Hammer, G. L., Podlich, D. W. & Messina, C. Modeling QTL for complex traits: detection and context for plant breeding. Curr. Opin. Plant Biol. 12, 231–240 (2009).

    CAS  Google Scholar 

  21. 21.

    Tardieu, F. & Tuberosa, R. Dissection and modelling of abiotic stress tolerance in plants. Curr. Opin. Plant Biol. 13, 206–212 (2010).

    Google Scholar 

  22. 22.

    Zhu, J. K. Abiotic stress signaling and responses in plants. Cell 167, 313–324 (2016).

    CAS  PubMed Central  PubMed  Google Scholar 

  23. 23.

    Hu, H. & Xiong, L. Genetic engineering and breeding of drought-resistant crops. Annu. Rev. Plant Biol. 65, 715–741 (2014).

    CAS  Google Scholar 

  24. 24.

    Roy, S. J., Negrao, S. & Tester, M. Salt resistant crop plants. Curr. Opin. Biotechnol. 26, 115–124 (2014).

    CAS  Google Scholar 

  25. 25.

    Rothstein, S. J., Bi, Y. M., Coneva, V., Han, M. & Good, A. The challenges of commercializing second-generation transgenic crop traits necessitate the development of international public sector research infrastructure. J. Exp. Bot. 65, 5673–5682 (2014).

    CAS  Google Scholar 

  26. 26.

    GM crops: a story in numbers. Nature 497, 22–23 (2013).

  27. 27.

    Petitions for Determination of Nonregulated Status (USDA, 2018); https://www.aphis.usda.gov/aphis/ourfocus/biotechnology/permits-notifications-petitions/petitions/petition-status

  28. 28.

    Amtmann, A. Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Mol. Plant 2, 3–12 (2009).

    CAS  PubMed Central  PubMed  Google Scholar 

  29. 29.

    Reef, R. & Lovelock, C. E. Regulation of water balance in mangroves. Ann. Bot. 115, 385–395 (2015).

    CAS  Google Scholar 

  30. 30.

    Munns, R. & Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651–681 (2008).

    CAS  Google Scholar 

  31. 31.

    Brown, G. W. Desert Biology Special Topics on the Physical and Biological Aspects of Arid Regions (Elsevier, Burlington, 2013).

  32. 32.

    Gechev, T. S., Dinakar, C., Benina, M., Toneva, V. & Bartels, D. Molecular mechanisms of desiccation tolerance in resurrection plants. Cell. Mol. Life Sci. 69, 3175–3186 (2012).

    CAS  Google Scholar 

  33. 33.

    Gaff, D. F. & Oliver, M. The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Funct. Plant Biol. 40, 315–328 (2013).

    Google Scholar 

  34. 34.

    Porembski, S. in Plant Desiccation Tolerance (eds Luttge, U. Beck, E. & Bartels, D.) 139–156 (Blackwell Publishing, Oxford, 2011).

  35. 35.

    Mitra, J., Xu, G., Wang, B., Li, M. & Deng, X. Understanding desiccation tolerance using the resurrection plant Boea hygrometrica as a model system. Front. Plant Sci. 4, 446 (2013).

    PubMed Central  PubMed  Google Scholar 

  36. 36.

    Griffiths, C. A., Gaff, D. F. & Neale, A. D. Drying without senescence in resurrection plants. Front. Plant Sci. 5, 36 (2014).

    PubMed Central  PubMed  Google Scholar 

  37. 37.

    Williams, B. et al. Trehalose accumulation triggers autophagy during plant desiccation. PLoS Genet. 11, e1005705 (2015).

    PubMed Central  PubMed  Google Scholar 

  38. 38.

    Asami, P., Mundree, S. & Williams, B. Saving for a rainy day: control of energy needs in resurrection plants. Plant Sci. 271, 62–66 (2018).

    CAS  Google Scholar 

  39. 39.

    VanBuren, R. et al. Single-molecule sequencing of the desiccation-tolerant grass Oropetium thomaeum. Nature 527, 508–511 (2015).

    CAS  Google Scholar 

  40. 40.

    Xiao, L. et al. The resurrection genome of Boea hygrometrica: a blueprint for survival of dehydration. Proc. Natl Acad. Sci. USA 112, 5833–5837 (2015).

    CAS  Google Scholar 

  41. 41.

    Costa, M. D. et al. A footprint of desiccation tolerance in the genome of Xerophyta viscosa. Nat. Plants 3, 17038 (2017).

    CAS  Google Scholar 

  42. 42.

    VanBuren, R. et al. Seed desiccation mechanisms co-opted for vegetative desiccation in the resurrection grass Oropetium thomaeum. Plant Cell Environ. 40, 2292–2306 (2017).

    CAS  Google Scholar 

  43. 43.

    Farrant, J. M. & Moore, J. P. Programming desiccation-tolerance: from plants to seeds to resurrection plants. Curr. Opin. Plant Biol. 14, 340–345 (2011).

    CAS  Google Scholar 

  44. 44.

    Land and Water (FAO, 2018); http://www.fao.org/land-water/en/

  45. 45.

    Flowers, T. J., Galal, H. K. & Bromham, L. Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct. Plant Biol. 37, 604–612 (2010).

    Google Scholar 

  46. 46.

    Flowers, T. J., Santos, J., Jahns, M., Warburton, B. & Reed, P. eHALOPH - Halophytes Database (Univ. Sussex, 2018); https://www.sussex.ac.uk/affiliates/halophytes/

  47. 47.

    Bromham, L. Macroevolutionary patterns of salt tolerance in angiosperms. Ann. Bot. 115, 333–341 (2015).

    CAS  Google Scholar 

  48. 48.

    Bromham, L. & Bennett, T. H. Salt tolerance evolves more frequently in C4 grass lineages. J. Evol. Biol. 27, 653–659 (2014).

    CAS  Google Scholar 

  49. 49.

    Flowers, T. J. & Colmer, T. D. Salinity tolerance in halophytes. New. Phytol. 179, 945–963 (2008).

    CAS  Google Scholar 

  50. 50.

    Inan, G. et al. Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol. 135, 1718–1737 (2004).

    CAS  PubMed Central  PubMed  Google Scholar 

  51. 51.

    Amtmann, A., Bohnert, H. J. & Bressan, R. A. Abiotic stress and plant genome evolution. Search for new models. Plant Physiol. 138, 127–130 (2005).

    CAS  PubMed Central  PubMed  Google Scholar 

  52. 52.

    Oh, D. H. et al. Loss of halophytism by interference with SOS1 expression. Plant Physiol. 151, 210–222 (2009).

    CAS  PubMed Central  PubMed  Google Scholar 

  53. 53.

    Yang, R. et al. The reference genome of the halophytic plant Eutrema salsugineum. Front. Plant Sci. 4, 46 (2013).

    CAS  PubMed Central  PubMed  Google Scholar 

  54. 54.

    Wu, H. J. et al. Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc. Natl Acad. Sci. USA 109, 12219–12224 (2012).

    CAS  Google Scholar 

  55. 55.

    Dassanayake, M. et al. The genome of the extremophile crucifer Thellungiella parvula. Nat. Genet. 43, 913–918 (2011).

    CAS  PubMed Central  PubMed  Google Scholar 

  56. 56.

    Plant Uses / Edible (PFAF); https://pfaf.org/User/edibleuses.aspx

  57. 57.

    Proches, S., Wilson, J. R. U., Vamosi, J. C. & Richardson, D. M. Plant diversity in the human diet: weak phylogenetic signal indicates breadth. Bioscience 58, 151–159 (2008).

    Google Scholar 

  58. 58.

    Biodiversity: Plants (FAO); http://www.fao.org/biodiversity/components/plants/en/

  59. 59.

    Miller, N. F., Spengler, R. N. & Frachetti, M. Millet cultivation across Eurasia: Origins, spread, and the influence of seasonal climate. Holocene 26, 1566–1575 (2016).

    Google Scholar 

  60. 60.

    Goron, T. L. & Raizada, M. N. Genetic diversity and genomic resources available for the small millet crops to accelerate a New Green Revolution. Front. Plant Sci. 6, 157 (2015).

    PubMed Central  PubMed  Google Scholar 

  61. 61.

    Bazile, D., Jacobsen, S. E. & Verniau, A. The global expansion of quinoa: trends and limits. Front. Plant Sci. 7, 622 (2016).

    PubMed Central  PubMed  Google Scholar 

  62. 62.

    Habiyaremye, C. et al. Proso Millet (Panicum miliaceum L.) and its potential for cultivation in the Pacific Northwest, U. S.: a review. Front. Plant Sci. 7, 1961 (2016).

    Google Scholar 

  63. 63.

    Theisen, A. A., Knox, E. G., Mann, F. L., Sprague, H. B. (eds). Feasibility of Introducing Food Crops Better Adapted to Environmental Stress 2 (National Science Foundation, Directorate for Applied Science and Research Applications, Division of Applied Research, Washington DC, 1978; 168–172.

    Google Scholar 

  64. 64.

    Miao, Z. Z. et al. Principal component analysis on traits related to yield and quality of hybrid millet. J. Shanxi. Agr. Sci. 41, 785–788 (2013).

    Google Scholar 

  65. 65.

    Bennetzen, J. L. et al. Reference genome sequence of the model plant Setaria. Nat. Biotechnol. 30, 555–561 (2012).

    CAS  Google Scholar 

  66. 66.

    Zhang, G. et al. Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat. Biotechnol. 30, 549–554 (2012).

    CAS  Google Scholar 

  67. 67.

    Jia, G. et al. A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nat. Genet. 45, 957–961 (2013).

    CAS  Google Scholar 

  68. 68.

    Varshney, R. K. et al. Pearl millet genome sequence provides a resource to improve agronomic traits in arid environments. Nat. Biotechnol. 35, 969–976 (2017).

    CAS  Google Scholar 

  69. 69.

    Hariadi, Y., Marandon, K., Tian, Y., Jacobsen, S. E. & Shabala, S. Ionic and osmotic relations in quinoa (Chenopodium quinoa Willd.) plants grown at various salinity levels. J. Exp. Bot. 62, 185–193 (2011).

    CAS  Google Scholar 

  70. 70.

    Zou, C. et al. A high-quality genome assembly of quinoa provides insights into the molecular basis of salt bladder-based salinity tolerance and the exceptional nutritional value. Cell Res. 27, 1327–1340 (2017).

    CAS  PubMed Central  PubMed  Google Scholar 

  71. 71.

    Yasui, Y. et al. Draft genome sequence of an inbred line of Chenopodium quinoa, an allotetraploid crop with great environmental adaptability and outstanding nutritional properties. DNA Res. 23, 535–546 (2016).

    CAS  PubMed Central  PubMed  Google Scholar 

  72. 72.

    Jarvis, D. E. et al. The genome of Chenopodium quinoa. Nature 542, 307–312 (2017).

    CAS  Google Scholar 

  73. 73.

    Clouse, J. W. et al. The Amaranth Genome: genome, transcriptome, and physical map assembly. Plant Genome. https://doi.org/10.3835/plantgenome2015.07.0062 (2016).

    Article  Google Scholar 

  74. 74.

    Yasui, Y. et al. Assembly of the draft genome of buckwheat and its applications in identifying agronomically useful genes. DNA Res. 23, 215–224 (2016).

    CAS  PubMed Central  PubMed  Google Scholar 

  75. 75.

    Zhang, L. et al. The tartary buckwheat genome provides insights into rutin biosynthesis and abiotic stress tolerance. Mol. Plant 10, 1224–1237 (2017).

    CAS  Google Scholar 

  76. 76.

    Ho, W. K. et al. Use of microsatellite markers for the assessment of bambara groundnut breeding system and varietal purity before genome sequencing. Genome 59, 427–431 (2016).

    CAS  Google Scholar 

  77. 77.

    Castaneda-Alvarez, N. P. et al. Global conservation priorities for crop wild relatives. Nat. Plants 2, 16022 (2016).

    Google Scholar 

  78. 78.

    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).

    CAS  PubMed Central  PubMed  Google Scholar 

  79. 79.

    Altieri, M. A., Nicholls, C. I., Henao, A. & Lana, M. A. Agroecology and the design of climate change-resilient farming systems. Agron. Sustain. Dev. 35, 869–890 (2015).

    Google Scholar 

  80. 80.

    Garibaldi, L. A. et al. Farming approaches for greater biodiversity, livelihoods, and food security. Trends Ecol. Evol. 32, 68–80 (2017).

    Google Scholar 

  81. 81.

    Rasmussen, C., Lagnaoui, A. & Esbjerg, P. Advances in the knowledge of quinoa pests. Food Rev. Intl. 19, 61–75 (2003).

    Google Scholar 

  82. 82.

    Khoury, C. K. et al. Increasing homogeneity in global food supplies and the implications for food security. Proc. Natl Acad. Sci. USA 111, 4001–4006 (2014).

    CAS  Google Scholar 

  83. 83.

    Cordain, L. et al. Origins and evolution of the Western diet: health implications for the 21st century. Am. J. Clin. Nutr. 81, 341–354 (2005).

    CAS  Google Scholar 

  84. 84.

    Pilbeam, D. J. Breeding crops for improved mineral nutrition under climate change conditions. J. Exp. Bot. 66, 3511–3521 (2015).

    CAS  Google Scholar 

  85. 85.

    Saleh, A. S. M., Zhang, Q., Chen, J. & Shen, Q. Millet grains: nutritional quality, processing, and potential health benefits. Compr. Rev. Food. Sci. F. 12, 281–295 (2013).

    CAS  Google Scholar 

  86. 86.

    Nowak, V., Du, J. & Charrondiere, U. R. Assessment of the nutritional composition of quinoa (Chenopodium quinoa Willd.). Food Chem. 193, 47–54 (2016).

    CAS  Google Scholar 

  87. 87.

    Martinez-Outschoorn, U. E., Peiris-Pages, M., Pestell, R. G., Sotgia, F. & Lisanti, M. P. Cancer metabolism: a therapeutic perspective. Nat. Rev. Clin. Oncol. 14, 11–31 (2017).

    CAS  Google Scholar 

  88. 88.

    Maddocks, O. D. K. et al. Modulating the therapeutic response of tumours to dietary serine and glycine starvation. Nature 544, 372–376 (2017).

    CAS  Google Scholar 

  89. 89.

    Knott, S. R. V. et al. Asparagine bioavailability governs metastasis in a model of breast cancer. Nature 554, 378–381 (2018).

    CAS  Google Scholar 

  90. 90.

    Popkin, B. M., Adair, L. S. & Ng, S. W. Global nutrition transition and the pandemic of obesity in developing countries. Nutr. Rev. 70, 3–21 (2012).

    PubMed Central  PubMed  Google Scholar 

  91. 91.

    Meyer, R. S. & Purugganan, M. D. Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14, 840–852 (2013).

    CAS  Google Scholar 

  92. 92.

    Lenser, T. & Theissen, G. Molecular mechanisms involved in convergent crop domestication. Trends Plant Sci. 18, 704–714 (2013).

    CAS  Google Scholar 

  93. 93.

    Hedden, P. The genes of the Green Revolution. Trends Genet. 19, 5–9 (2003).

    CAS  Google Scholar 

  94. 94.

    The cost of sequencing a human genome. NIH https://www.genome.gov/sequencingcosts/ (2016).

  95. 95.

    Goodwin, S., McPherson, J. D. & McCombie, W. R. Coming of age: ten years of next-generation sequencing technologies. Nat. Rev. Genet. 17, 333–351 (2016).

    CAS  Google Scholar 

  96. 96.

    Carvalho, A. B., Dupim, E. G. & Goldstein, G. Improved assembly of noisy long reads by k-mer validation. Genome Res. 26, 1710–1720 (2016).

    CAS  PubMed Central  PubMed  Google Scholar 

  97. 97.

    IWGSC et al. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361, eaar7191 (2018).

    Google Scholar 

  98. 98.

    Yin, K., Gao, C. & Qiu, J. L. Progress and prospects in plant genome editing. Nat. Plants 3, 17107 (2017).

    CAS  Google Scholar 

  99. 99.

    Zhang, H., Zhang, J. S., Lang, Z. B., Botella, J. R. & Zhu, J. K. Genome editing-principles and applications for functional genomics research and crop improvement. Crit. Rev. Plant. Sci. 36, 291–309 (2017).

    Google Scholar 

  100. 100.

    Miki, D., Zhang, W., Zeng, W., Feng, Z. & Zhu, J. K. CRISPR/Cas9-mediated gene targeting in Arabidopsis using sequential transformation. Nat. Commun. 9, 1967 (2018).

    PubMed Central  PubMed  Google Scholar 

  101. 101.

    Hua, K., Tao, X., Yuan, F., Wang, D. & Zhu, J. K. Precise A.T to G.C base editing in the rice genome. Mol. Plant 11, 627–630 (2018).

    CAS  Google Scholar 

  102. 102.

    Lowe, K. et al. Morphogenic regulators baby boom and wuschel improve monocot transformation. Plant Cell 28, 1998–2015 (2016).

    CAS  PubMed Central  PubMed  Google Scholar 

  103. 103.

    Zhao, X. et al. Pollen magnetofection for genetic modification with magnetic nanoparticles as gene carriers. Nat. Plants 3, 956–964 (2017).

    CAS  Google Scholar 

  104. 104.

    Cunningham, F. J., Goh, N. S., Demirer, G. S., Matos, J. L. & Landry, M. P. Nanoparticle-mediated delivery towards advancing plant genetic engineering. Trends Biotechnol. 36, 882–897 (2018).

    CAS  Google Scholar 

  105. 105.

    Watson, A. et al. Speed breeding is a powerful tool to accelerate crop research and breeding. Nat. Plants 4, 23–29 (2018).

    Google Scholar 

  106. 106.

    Borlaug, N. E. Nobel lecture: the Green Revolution, peace, and humanity. The Nobel Prize https://www.nobelprize.org/prizes/peace/1970/borlaug/lecture/ (1970).

  107. 107.

    Wang, W. et al. Cassava genome from a wild ancestor to cultivated varieties. Nat. Commun. 5, 5110 (2014).

    CAS  PubMed Central  PubMed  Google Scholar 

  108. 108.

    Wang, M. et al. The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication. Nat. Genet. 46, 982–988 (2014).

    CAS  Google Scholar 

  109. 109.

    Monat, C. et al. De novo assemblies of three Oryza glaberrima accessions provide first insights about pan-genome of African rices. Genome Biol. Evol. 9, 1–6 (2017).

    Google Scholar 

  110. 110.

    Zhang, Y. et al. Genome and comparative transcriptomics of African wild rice Oryza longistaminata provide insights into molecular mechanism of rhizomatousness and self-incompatibility. Mol. Plant 8, 1683–1686 (2015).

    CAS  Google Scholar 

  111. 111.

    Mondal, T. K., Rawal, H. C., Gaikwad, K., Sharma, T. R. & Singh, N. K. First de novo draft genome sequence of Oryza coarctata, the only halophytic species in the genus. Oryza. F1000Res 6, 1750 (2017).

    Google Scholar 

  112. 112.

    Aversano, R. et al. The Solanum commersonii genome sequence provides insights into adaptation to stress conditions and genome evolution of wild potato relatives. Plant Cell 27, 954–968 (2015).

    CAS  PubMed Central  PubMed  Google Scholar 

  113. 113.

    Ming, R. et al. The pineapple genome and the evolution of CAM photosynthesis. Nat. Genet. 47, 1435–1442 (2015).

    CAS  PubMed Central  PubMed  Google Scholar 

  114. 114.

    Ma, T. et al. Genomic insights into salt adaptation in a desert poplar. Nat. Commun. 4, 2797 (2013).

    Google Scholar 

Download references

Acknowledgements

We would like to thank H. Zhang and R. Bressan for careful reading and editing of the manuscript. Research funding was provided by the Chinese Academy of Sciences (CAS) to J.K.Z. and by Strategic Priority Research Program of the Chinese Academy of Sciences (XDB27040108), Shanghai Science and Technology Committee (17391900200), Youth Innovation Promotion Association of CAS (2014242), National Key R&D Program of China (2016YFA0503200) and CAS to H.Z.

Author information

Affiliations

Authors

Contributions

H.Z. and J.K.Z. wrote the paper; H.Z. and Y.L. analysed data.

Corresponding authors

Correspondence to Heng Zhang or Jian-Kang Zhu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, H., Li, Y. & Zhu, J. Developing naturally stress-resistant crops for a sustainable agriculture. Nature Plants 4, 989–996 (2018). https://doi.org/10.1038/s41477-018-0309-4

Download citation

Further reading